I. OVERVIEWF. A. Mote
II. CENTRAL MECHANISMSRagnar Granit
In any consideration of behavior it is important to have knowledge of the senses, for the first step in an organism’s adjustment to its environment is sensory stimulation. The behavior of primitive organisms is simple and limited; this is so partly because their receiving mechanisms are of such a nature and so structured that the organisms can sense only gross changes in their restricted environment. Higher forms of life have more numerous, more complex, and more sensitive mechanisms; therefore, it is possible for them to react to more environmental changes as well as to changes of wider range and greater subtlety. At the human level the mechanisms have become so specialized, and the environment is so complex, that to understand much of man’s most significant behavior, it is necessary to know about the receptor systems by which he senses and adjusts to his varied and changing world.
Classification of senses
Although it is popularly believed there are only five senses, there are actually more. No specific number can be stated because it will vary from one listing to another, depending upon the criteria used to classify the senses. A set of criteria often used consists of the kind of subjective experience involved–visual, olfactory, tactile, etc.–the type of stimulus, and the sense organ, or receptor. Table 1 outlines this scheme.
The nature of sensory experiences
The stimulation of a sense organ results in a unique kind of experience, and the differences in kind are what we identify in speaking of auditory, taste, and other types of sensations. The traditional five senses of sight, hearing, taste, smell, and touch have been defined this way since the time of Aristotle, but it has long been known that these do not make the complete list, since sensations of warmth, cold, heat, and pain–in addition to
|Table 1 Scheme for classifying senses|
|Vision||Electromagnetic radiations||Rods and cones of the retina|
|Hearing||Pressure of sound waves||Hair cells of the organ of Corti of the inner ear|
|Taste||Various substances in solution||Taste cells in taste buds of the tongue|
|Smell||Various vaporized materials||Bipolar neurons of olfactory nerve in olfactory epithelium in upper nasal cavity|
|Touch||Deformation of skin, mucous membrane, internal organs, etc., by stretching, pulling, and similar stimulation||Free nerve endings|
|Pressure (“deep,” i.e., subcutaneous and internal pressure)||Pressure in excess of that required for touch, distension of internal organs, etc.||Pacinian corpuscles in subcutaneous tissue and internal organs|
|Warmth||Contact by stimulus above “physiological zero,” radiant heat, elevation of temperature of surrounding medium||Receptor uncertain or disputed|
|Cold||Contact by stimulus below “physiological zero” lowering of temperature of surrounding medium||Receptor uncertain or disputed|
|Pain||Various electrical, thermal, mechanical, chemical, and other agents, e.g., electric shock, radiant heat, puncture, some acids, etc.||Free nerve endings|
|Vestibular (equilibrium, labyrinthine)||Linear and rotational acceleration, head and body position and movement||Cristae of semicircular canals and otoliths of macula of utricle and sacule (all parts of nonauditory portion of inner ear)|
|Kinesthesis (movement and “muscle sense”)||Movement of muscles, tendons, and joints||Various receptors in muscles, tendons, and joints, e.g., spray-type nerve endings and free nerve endings in muscular tissue and joints, Golgi tendon organs, modified Pacinian corpuscles|
touch–can be aroused when the skin is stimulated. Even when these are included, the list is still far too short because movement, pressure, fatigue, nausea, and many others that could be named are experienced as sensations just as much as, let us say, taste and sight. In addition to the differences in kind of sensation from one sense to another, there are also differences in quality within each sense. Not only is taste as a class of sensations different from sight, but the taste quality of sweetness is different from that of sourness, and the visual quality of whiteness different from that of other colors. The number of sensations and their variations and combinations is infinite. To order the domain of the sensations, Hermann von Helm-holtz introduced the concept of modality, which is defined as the class of sensations, all of which are alike.
The basic aspects of sensation are intensity, sensory modality, and sensory quality. First, let us briefly consider sensation intensity. Most sense organs are specialized; that is, they are composed of receptor elements whose threshold of excitability is lower for one form of energy than for any other. This particular type of energy is known as the adequate stimulus. Receptors will react to other stimuli–for example, the application of an electric current or pressure on the eyeball will arouse visual sensations–but the energy required is greater; such stimuli are often referred to as inadequate.
Absolute threshold. The minimum amount of the adequate stimulus necessary to excite a sense organ is called the absolute threshold. For some senses the energy required is extremely small; for instance, at the absolute threshold for human vision the rods can respond when they absorb only 6–10 light quanta, and it has been calculated that movements of the eardrum of the order of 109 cm. can excite the auditory system.
Differential threshold. The senses, however, do more than detect the presence or absence of stimulation; they respond to differences in stimulus magnitude. As the value of the stimulus is increased above the absolute threshold, the sensation experienced becomes more intense–the light becomes brighter and the sound louder. But it is also important to know how much difference there must be so that one light can be seen as brighter than another or what change in sound frequency is required in order to be able to recognize that two tones differ. This is the problem of the differential threshold, defined as the just noticeable difference in stimulation. The size of the differential threshold is a measure of receptor sensitivity; when the just noticeable difference is small, sensitivity is high, when this difference is large, sensitivity is low.
Work of Weber and Fechner. E. H. Weber’s research in the 1830s and 1840s led him to conclude that the just noticeable difference in stimulus intensities, ΔI, depends upon the ratio of their magnitudes, that is, ΔI = I1/I2, and that for a given class of stimuli the ratio is constant. Thus, if a light intensity of 11 units can be discriminated as just noticeably brighter than one of 10 units, then a light intensity must be of 110 units to be discriminated from one of 100 units, and so on–the constant ratio being 1/10 in this example. Although he knew the value of the ratio varied from one class of stimuli to another, Weber believed it was constant for any given class, a generalization that has usually been found to hold true for only a part of the total range of magnitude for any stimulus class. Gustav Fechner applied Weber’s findings about intensities of stimuli to intensities of sensation, assuming that a just noticeable increase in stimulus intensity meant there was a constant increment in sensation intensity. He believed the quantitative relationship between stimulus and sensation was logarithmic, and in 1860 he expressed this in his famous psychophysical law: S = k log I, where S is sensation intensity and I is stimulus intensity (Boring 1942). [A more detailed treatment of thresholds, the relationship between stimulus magnitude and sensation intensity, and the problems and methods involved in their measurement will be found in Psychophysics; see also the biographies of Fechner and Weber, ErnstHeinrich.]
Although the importance of sensation intensity has always been recognized, most of the interest in the senses has centered about the problems of sensory modality and the quality differences within a modality. Our daily experiences seem to provide the answer to the question “What is there about the stimulus, the sense organ, or the nervous system that explains sensory modality?” To common sense it appears self-evident that, although the nervous system transmits neural activity to the brain, where sensory experience occurs, the essential factor that accounts for sensory modality is the stimulus-sense organ relationship. This determines which experience takes place in the brain. Thus, the color of the grass stimulates the eye, and we have the sensation of greenness; the singing of the bird falls on the ear, and we hear; the skin senses the warmth of the sunshine and the cool of the shade. In order to experience a particular sensation, it is simply a matter of the natural stimulus exciting the appropriate sense organ.
However, it is not only the “natural” stimulus that can arouse a given sensation. For example, a blow on the head will evoke visual sensations and make the ears ring; the usual stimulus for dizziness is spinning or rotating the body, but rotating the visual field will have the same effect; a very warm stimulus may be felt as cold when applied to a cold-sensitive spot on the skin–the “paradoxical cold” phenomenon. These examples demonstrate an important fact: no matter how it is excited, whenever a specific sense organ is stimulated, the sensation is always the same. Yet it is not necessary for the sense organ itself to be stimulated in order for its appropriate modality of sensation to be experienced. For instance, when the optic nerve is cut, a flash of light is seen, and after amputation of an arm there may be reports of touch, itching, pain, and other sensations that are felt as coming from the missing hand and fingers. [SeeBody Image.]
Doctrine of specific nerve energies. If neither a particular stimulus nor stimulation of a particular sense organ is essential, then there must be something about the nervous system that is the necessary factor determining sensory modality. It is this conclusion that Johannes Muller stated in his doctrine, or law, of specific nerve energies (Boring 1942). It was M tiller’s hypothesis that each sensory nerve has its unique “energy,” or quality. Miiiler’s hypothesis declares that sound is sensed because of the unique specific energy of the auditory nerve, smell because of the specific energy of the olfactory nerve, and the other sense modalities because of similar specific energies–and the modalities differ because the specific nerve energies are different. Although no property of sensory nerves has ever been found which supports the specific-energy concept, Miiller’s doctrine has been very influential in theory and research upon the senses. It led investigators to look for specialized receptors which, when they activate their sensory nerve, arouse a particular type of sensation [SeeMuller, Johannes].
Problem of special receptors. For most of the senses an interrelationship can be found which involves an adequate stimulus, a specialized receptor, and a specific modality of sensation. Light stimulates the rods and cones of the retina, and we see; substances stimulate the taste buds of the tongue, and we taste. Relations of this sort can be found for many modalities. However, such information about some senses is uncertain, and our knowledge of how sensations evoked by stimulation of the skin are mediated is an example of this. The skin is not uniformly sensitive but has “spots” of sensitivity that respond to touch, temperature, etc. Under most conditions no temperature is felt at a given cutaneous region; it is at “physiological zero.” Upon being stimulated point by point by a stimulus above this zero value, warmth is not felt at all points nor is cold when a stimulus below this value is used; warm and cold sensations are only reported upon stimulation at certain spots, and the number and location of these are different for the two kinds of stimuli. This finding has been interpreted as indicating the existence of a special receptor for warmth and a different one for cold at each temperature-sensitive spot. A similar interpretation has been proposed for touch, one type of receptor to serve for hairy skin and another type for hairless. Because of their number and nearness to pain-sensitive spots, the free nerve endings are considered to mediate pain. Although the free nerve endings usually are not considered to be specialized receptors, when they are appropriately stimulated, touch and temperature will also be sensed (Weddell 1955).
The cutaneous senses have sometimes been discussed in terms of a conception of modality which implicitly assumes there must be four morphologically distinct types of receptors. But the fact that all the cutaneous modalities can be evoked by stimulating the free nerve endings casts doubt upon the necessity to assume distinct receptor types. The meaning of cutaneous sensation also requires clarification. “Touch,” “warmth,” “cold,” and “pain” do not designate unique sensations perceived in isolation; such terms refer to the predominant experience aroused by particular stimuli. A stimulus above physiological zero applied to the skin evokes warmth as the primary feeling, but the stimulus is also felt as a touch at a particular location, and it is perceived as having temporal and spatial characteristics. This example also illustrates an important phenomenon, that of sensory interaction. The inputs from sensory systems interact at the higher nervous centers and are integrated there so as to give us our perceptions of the environment. [SeeSkin Senses And Kinesthesis.]
To speak of sensation is also to speak of sensation quality; the two are inseparable. Visual sensations are white, or gray, or red, or yellow; a pain is “dull,” or “aching,” or “throbbing”; and similarly for all the senses. The usual method of investigating sensory quality has been to search for the aspects of the stimulus which correlate with quality and variations in quality. For many of the senses some of the most important correlations are known and the factors involved have been studied for many years. For vision the wave length of the light and color quality are correlated; sound frequency correlates with pitch, and the pattern of overtones with the characteristic timbre of musical instruments and the voice; lightly stroking the skin evokes the touch quality of tickling, and so on. Much of our knowledge about the senses consists of information of this sort, and many of the most important generalizations and theories about the senses, such as the Young-Helmholtz theory of color vision and the place theory of pitch for hearing, are explanations of sensory quality [SeeHelmholtz].
Receptor-quality correlations. Obviously, before there can be any satisfactory scientific understanding, the receptor and the quality that are involved in the stimulus-quality correlation must be known. For some senses our knowledge about one or the other of these is questionable. In the case of thermal sensitivity the stimulation is temperature above or below physiological zero, and the sensory quality is warmth or cold, but since there is uncertainty about how thermal sensitivity is mediated, little that is conclusive can be said about any correlation. In the case of olfaction there is the opposite difficulty; here there is no question about the receptor, but anywhere from three to nine classes of odor qualities have been proposed. Since agreement has not been reached about the analysis of the qualities, here too no satisfactory stimulus-quality correlation can be established.
Localization in the brain. When it became clear that Miiller’s specific nerve-energy concept was not tenable, the only reasonable alternative hypothesis seemed to be one which he had considered as a possibility, namely, that when a sense organ is stimulated, its sensory nerve sets up excitation in a particular region in the brain; there is specificity because nerves from different sense organs go to different regions. Specificity does exist in the sense that the optic-nerve radiations terminate in the occipital lobe of the brain, and hence this is the visual center; the auditory nerve ends in the temporal region, and this is the auditory center, and so on. However, although occasionally someone has entertained the possibility of something like them, no “green center,” “warm center,” or “center” for sweet tastes or flowery odors and the like has been found. Such a conception of specificity is too simple.
Methods and findings
Within this century the most significant contributions to the understanding of the senses have come from electrophysiological investigations. By appropriate techniques the responses of individual receptors and of single nerve fibers can be studied as the stimuli are varied. Under most conditions of stimulation the electrical changes recorded from a single nerve unit are a series of discharges, all of the same size, and the unit is therefore said to show all-or-none response. As intensity of stimulation is increased or decreased, it is not the magnitude of discharge of the nerve that varies, but its frequency; and when records are taken from several units, it is found that variation in stimulus intensity is also reflected in the number of units responding. The frequency of unit discharge and the number of units excited are considered to be the basic neural correlates of the dimension of sensation intensity.
Recent research on the electrophysiology of taste has provided data and information which show that some of the ways of looking upon sensation and sensation quality must be reconsidered. That the taste cell of the taste bud is the receptor for taste has long been known, and although from time to time different classifications of primary taste qualities have been proposed, it was finally agreed that there are four: sour, salty, sweet, and bitter. Most of the taste buds are found in small elevations on the tongue known as papillae. Individual papillae have been found which respond exclusively to salt, to sour, and to sweet, but most are stimulated by substances which evoke more than one quality. Recordings have been made of the electrical activity of single units of the nerves supplying various animal taste buds when these are being stimulated by weak acids, sodium chloride, sugar, quinine, and other substances that evoke the different primary taste qualities in the human subject. Such records show that most units respond to more than one substance, and from one unit to another there is variation in the degree of response to different substances. For example, one unit might respond to both hydrochloric acid and sodium chloride, but in a different degree to each; another unit might respond to the same concentration of these, but to another degree for each, and in addition it might respond to quinine. A third unit might, again, respond to both the acid and the salt at the same concentration, and to still a different degree for each, and to sucrose as well. Thus, although many units may respond to stimuli for the primary taste qualities, each may have its own response “spectrum,” or characteristic pattern of sensitivity. Such findings do not support a simple view of four basic receptor-cell or nerve-unit types corresponding to the four taste qualities. “Sweet,” “sour,” etc. are probably best considered as descriptive headings for taste qualities, rather than as terms signifying any sort of entity. It appears then that neither the responses of individual cells nor of single neural units determine taste quality—it is the patterning of sensory nerve activity which provides the basis for taste discrimination (Pfaffmann 1962).
Electrophysiological methods have been used to investigate the individual receptor elements, the nerve pathways, and the cortical centers for all the senses; information that could have been obtained in no other way has been gathered. By such methods new discoveries have been made which show that some of the traditional views and theories about the senses are too simple and inadequate. [SeeNervous System, article on Electroenceph Alography.]
In the past the senses were studied for the purpose of explaining sensations and their qualities. Now there is less emphasis on this, and the senses are being studied in and for themselves in order to gain knowledge about their properties and their processes. Work undertaken with this new purpose is not only giving us better knowledge of sensations and qualities but it is also giving us a larger view of the senses and the part they play in the behavior of organisms.
F. A. Mote
[Directly related are the entriesHearing; Pain; Skin Senses And Kinesthesis; Taste And Smell; Vlsion. Other relevant material may be found inAttention; Nervous System, article on Structure And Function OF The Brain; Psychophysics; and in the biographies ofFechner; Helmholtz; Hering; Muller, Johannes; Weber, Ernst Heinrich; Wundt.]
Boring, Edwin G. 1942 Sensation and Perception in the History of Experimental Psychology. New York: Appleton.
Geldard, Fkank A. 1953 The Human Senses. New York: Wiley.
Pfaffman, Carl 1962 Sensory Processes and Their Relation to Behavior: Studies on the Sense of Taste as a Model S-R System. Volume 4, pages 380–416 in Sigmund Koch (editor), Psychology: A Study of A Science. New York: McGraw-Hill.
Piehon, Henri (1945) 1952 The Sensations: Their Functions, Processes, and Mechanisms. New Haven: Yale Univ. Press; London: Miiller. → First published as Aux sources de la connaissance: La sensation, guide de vie.
Symposium ON Principles OF Sensory Communication, Endicott House, 1959 1961 Sensory Communication: Contributions. Cambridge, Mass.: M.I.T. Press.
Weddell, G. 1955 Somesthesis and the Chemical Senses. Annual Review of Psychology 6:119–136.
Physiology had very little precise information concerning central mechanisms of sensation until the advent of the micromethods of modern neuro-physiology. The well-known basic facts concerning specific cortical projection areas for vision, hearing, etc., more properly belong to the conceptual sphere of functional anatomy and pathology. This article will attempt to make some sense out of the less accessible results dealing with the organization of sensory messages and their transmission as revealed by microtechniques in terms of single fibers and individual cells.
The central mechanisms of sensation come into operation at the first synapse which the neural message encounters on its way from the sense organ. In the eye and the ear, for instance, this synapse is located in the periphery at the base of the receptors themselves. For afferents leading from receptors in the skin, the synapse is found in the spinal cord and in its upper extension, the medulla oblongata. In the eye the message is twice reorganized before it reaches the optic nerve, at the synapse of the receptor and bipolar cells and at the synapse of the bipolar and ganglion cells. There, some “sharpening” of the information takes place, aided as we shall see, by the mobility of the eye. Skin and muscular afferents are synaptically connected in the spinal cord to elaborate reflex systems that in turn are controlled by internuncial cells (interneurons) run by centripetal circuits that can redirect, inhibit, or facilitate the passage of information.
The sense organs whose central mechanisms have been most carefully studied are the eye, the ear, and the muscle spindles. These will be used to illustrate some of the leading principles that have emerged from such work.
Let us first consider the extremely high sensitivity of the sense organs. If this sensitivity were always fully utilized and its effect transmitted to the cortex, the higher centers would be at the mercy of an impulse barrage that would depolarize their neurons to a level fatal for organized life. Obviously situations exist in which full sensitivity is needed, as in extreme twilight vision for the eye, or in the minute adjustments of muscle length made by the spindle organs. But the eye must also be able to function in brightest sunlight, and most muscular movements are coarse and would be disturbed by excessive spindle discharges, which as we know, are returned reflexively to the muscles in which these organs are situated. These two examples suffice to show that sensitivity must be regulated. Much of the most important work on central afferent mechanisms has been devoted to the elucidation of both local and distant (or centripetal) controlling mechanisms that act internally on the neurons or receptors themselves. These are distinct from well-known external mechanisms, such as pupillary reflexes and activities of the stapedius and tensor tympani muscles in the middle ear.
An important restrictive peripheral mechanism requiring brief mention is the adaptation of the receptors that is expressed in a reduction of impulse frequency as a function of the length of time of stimulation (Adrian 1928). The so-called light and dark adaptation of the retina is a borderline case: there is a peripheral shift from rod, or scotopic, vision based on rhodopsin to cone, or photopic, vision as the level of illumination increases, but neural mechanisms within the retinal center itself are also deeply engaged in the adaptive adjustments of the sensitivity of the eye. The details of their mode of operation are not as well known as one could desire. Their existence, however, is well established by several workers (summarized in Granit 1962).
Relays and transmission
At an earlier time, the different synaptic stations traversed by a message were regarded merely as relays, a loosely defined function quite apart from the complications alluded to above. We realize today that afferent messages from different receptors at a relaying neuron may be mixed in different ways by the manner in which their afferent terminals converge and that controlling mechanisms interfere at each station, either to specify, amplify, or partially or wholly block a message. Nevertheless, there is always some relay function involved, in the sense that even a modified impulse message must be transmitted to the next station with some fidelity as to its “quantity.” Since impulse frequency (in addition to the number of active cells) is a most important determinant of quantity or intensity, clearly there must be a mechanism for relaying it with a good margin of safety. One factor making a relay reasonably reliable is “synaptic density.” A relay could be made to transmit with an equal margin of safety without a dense synaptic projection, but in such systems facilitatory or inhibitory controls would be relatively more important in deciding under what circumstances maximum output would be permitted.
At each relay, impulse frequency is translated at the cell membrane into miniature synaptic currents which can be recorded (through microelectrodes introduced into the cell and connected to amplifiers) as miniature potentials (see Eccles 1957; 1964). These indicate depolarization when the input is excitatory and the opposite, or hyperpolarization, when the input is inhibitory. Several sense organs have both inhibitory and excitatory afferents, the classical example being the large spindle afferents with reciprocally connected inhibitory and excitatory terminals to the protagonist and antagonist ventral horn cells, respectively.
In an excitatory relay of substantial synaptic density, the miniature synaptic currents are in one direction, all depolarizing, and hence will produce a graded change, the depolarizing current, often recordable in terms of electrical potential. Eccles (1957; 1964) calls it the postsynaptic excitatory potential. It will be translated into an impulse discharge. Imitating this process by injecting current through the tip of an intracellular electrode, one finds impulse frequency directly proportional to current strength (Granit et al. 1963). At the next relay these impulses will produce an amount of excitatory current dependent upon the frequency of discharge and the synaptic density. Is this process also directly proportional to impulse frequency? Indirect evidence supports this proposition (see below). The relay function of an afferent neuron lying in the path of the message to the cortex thus consists in translating an impulse barrage into depolarizing current and that once again into an impulse barrage and so on alternately at each subsequent station. Since proportionality is maintained, the message can be transmitted without distortion of the relative order of magnitude. The lemniscal path seems to exhibit the simple relay function described (Mountcastle 1961). The proportionality constants relating depolarizing current strength to impulse frequency are known to vary, and thus if they happened to be large, a sensory effect could be stepped up by amplification; if not, the initial frequency of discharge may be reproduced at the end station in its original version.
When more complex functions are considered, the simple picture drawn above of a pure relay function ceases to be sufficient. Transmission will then be greatly influenced by internuncial cells that “take orders” from elsewhere. A large number of them characteristically fire rapid bursts of impulses when stimulated by a single shock. When tested for their impulse-producing capacity by injected currents, these cells have been proved to possess very large proportionality constants, meaning that very small amounts of current elicit fast frequencies of discharge. Such cells are therefore well suited for “biasing,” in the positive or negative direction, the relays upon which they impinge.
Specific and diffuse afferents
When a sense organ has to deliver specific information of a more discriminative nature referring to spatial localization or some modality, this information is arranged spatially with considerable precision both at intermediate and at end stations. Topographic differentiation by means of somatotopic afferents is thus a major analytical tool of the physiological organization by which input is differentiated. In vision the physiological maps are particularly precise. The eyes, for instance, are represented by alternate layers in the geniculate body in such a manner as to join corresponding points of the retinal field in identical layers. The information, thus organized, is delivered to a cortical map of great precision. For touch, Woolsey (1952) has worked out detailed cortical charts by the method of evoked potential. Even quality may in some systems be mapped out. This is the case in the cortical area for tonal representation (Tunturi 1950). Examples could be multiplied to show how information on the structure of bodily space is charted in this manner by localized signals.
Differentiation by the basic principle of maintaining the topography of sensory impulses from sense organ to cortex is, however, not the only afferent mechanism known. There are also cells which serve diffuse or nonspecific functions. This concept is not easy to define with precision. Perhaps the best way of defining a diffuse afferent system is to call it “a system of cells on each of which afferent fibers of several modalities converge,” or if the afferents be of one modality, “cells receiving projections from an extensive section or area of the body.” Magoun’s (1950) concept of the ascending reticular system is of the former type, in which neurons in the brain stem receive terminals from afferents representing a large number of different modalities, as proved in unit analysis by Moruzzi and his co-workers (Scheibel et al. 1955). Of the other type is the spinothalamic system, whose thalamic neurons have receptive fields which may include one half or the whole of the body (Mountcastle 1961). They may, however, have terminals from two modalities (if pain be a modality) because nociceptive stimuli also discharge the cells which are sensitive to mechanical stimulation of the skin. In the retina the giant ganglion cells have branches that collect information across an area with a diameter of maximally 1 mm., representing several hundred thousand receptors, both rods and cones. Within the tactile system of the gracilis nucleus of the dorsal-column afferents, there are separate cells for localized messages and for highly convergent information coming from a large area.
What function should be assigned to diffuse systems? Only a partial answer can be given. For the reticular activating system, Starzl, Taylor, and Magoun (1951) suggest (as does the name itself) that it plays the role of keeping the brain alert and active, since somnolence occurs when this portion of the brain stem is removed. Granit (1955), drawing attention to the widespread spontaneous activity of nerve cells, has made two suggestions: (1) that the diffuse sensory input serves an energizing function; that is, it maintains some basic depolarization by random impulses which is necessary for the upkeep of spontaneous activity in the higher centers; and (2) that spontaneous activity in its turn is necessary as a background for the central recognition of inhibition. As we shall see below, inhibition is necessary in discrimination, but it needs a background of central excitation in order to be “informative.” In studying intracellularly the afferent input from stretch receptors, we have been able to demonstrate (Granit et al. 1964) that, unless the cell (a motoneuron) is depolarized to some extent, both inhibitory and excitatory effects of stretch tend to be dissipated as sheer noise consisting of miniature potentials at the cell membrane, while in slightly depolarized cells, excitations really excite and inhibitions really inhibit.
The final cell
The neurophysiologist whose understanding depends on interpreting “spikes” (impulses) or membrane events (synaptic activation noise, membrane potential) has no experimentally based philosophy as to which, if any, of his indices comes close to the conceptual world of psychology. So far he has done best on spikes and has been tacitly inclined to imagine that unless a cortical cell delivers spikes, it is of but modest interest in the nervous machinery designed for discrimination of one message from another. Yet, while he is recording from the “final cell” in a cortical layer, no neurophysiologist is likely to believe that he is doing anything more than sampling one link in an organization of cortical cells that, according to the anatomist Ramόn y Cajal (1923), consists of a “cortical sector” (a “cone” would have been a more appropriate term) with its top downwards. Within this sector the cells are linked vertically. Physiological research (see below) has recently been able to make valuable use of Ramόn’s concept.
The role of inhibition
Impulse recording made it possible for the first time to assign definite tasks to nervous inhibition in the elaboration of the sensory message. Previously, central inhibition had been measurable only in reflex work, using muscular contraction or secretion as indices. Graded excitation (depolarizing current) has its equivalent antagonist in graded inhibition (hyperpolarizing current), often recordable by the intracellular technique as the “inhibitory postsynaptic potential” (Eccles 1957; 1964). However, most information of interest for the present theme has been obtained in terms of a reduction of impulse frequency.
Inhibition within a sensory system achieved functional prominence in the vertebrate retina for the first time when it was shown that the off-discharge at cessation of illumination was preceded by inhibition and easily inhibited by reillumination (Granit Therman 1935; Hartline 1938). The retina is our most highly developed sense organ, and if natural stimulation of it by light could stop a discharge as well as start it, then surely inhibition is of first importance. The on-off pattern of discharge delivered by the individual optic nerve fibers was later also seen in the auditory system (Bremer 1943). However, in vision its significance is far better understood, apparently because the spatial element of the organ of sight is more accessible to analysis. From the beginning it was held that the on-off units of the retina would blaze the trail of a moving object with a recognizable spike pattern and that, similarly, contours would be emphasized because both regular and small, irregular eye movements light it up with on-off spikes. It has since been shown in precise experiments (Ditchburn 1955) that if the image on the human retina is maintained stationary by appropriate optical arrangements compensating for slight, unavoidable eye movements, then it also tends to fade out.
The on-off element, and likewise a smaller number of pure “on” and pure “off” elements, represents a receptive field of convergence together with an analyzer residing in the nervous structure between receptors and the ganglion cell whose message is recorded. The size and organization of the receptive field were first studied, with the aid of small spots of light, by Hartline (1940) in the frog and then in the cat (Kuffler 1953), where they were found to be differentiated to the extent that they possess a center that is either “on” or “off.” In both cases the surrounding part of the field had the opposite character. In the goldfish the receptive field has also been investigated with respect to wave-length sensitivity, and it has been found that this antagonism between center and periphery with respect to on and off may also be an antagonism in terms of spectral regions of sensitivity. The overlapping mosaic of receptive fields thus forms a dynamic interaction pattern which, transmitted up the optic nerve, can do justice to the infinite variety of form, movement, and color that a moving animal has to interpret and that it ultimately reproduces in the form of a stable world of sight. In this act inhibition is just as vital as excitation.
Recurrent inhibition. Recurrent inhibition is another significant and apparently common process in the organization of the sensory (and motor) message because it rejects unwanted components, emphasizes differences of “quantity” within a complex message, and apparently also stabilizes a steady discharge. Its basis is the common occurrence in all centers of recurrent collateral fibers returning directly or across an interneuron to the cell or cell system from which the parent fiber emerged. Most of our knowledge of this process, inasmuch as it consists of precise measurements, derives from cells as different as vertebrate ventral horn cells and the horseshoe crab (Limulus) ommatidia. In the latter case (Hartline Ratliff 1958) the afferent large axon from each ommatidium sends fibers with inhibitory axo-axonic synapses to adjacent axons. Assume that an image is focused onto some ommatidia with irradiated light unavoidably spreading across surrounding ones. The ommatidia in focus will fire at higher frequencies than those in the surrounds. The recurrent inhibition has proved to be proportional to impulse frequency and hence the focal cells will inhibit those in the neighborhood more than the latter can inhibit them. As a consequence the image will be sharpened by “contrast.”
Nature has preserved, as it were, the idea of recurrent, or “lateral,” inhibition (in Hartline’s terminology) through countless ages of phylogenetic development; recurrent fibers are found in most centers, both motor and sensory. In the ventral horn cells (Granit & Renkin 1961), in addition to “motor contrast,” a stabilizing effect on the discharge frequency in tonically active cells can be demonstrated. While in the Limulus the mechanism appears to be wholly automatic, in the ventral horn cells it is provided with an internuncial neuron, the so-called Renshaw cell, and hence is facultative (for a summary, see Granit 1963).
These cases of recurrent inhibition are the only ones analyzed in detail, but further developments can be expected, since qualitative work has already been done, for instance, in the hippocampus, in the olfactory bulb, and in the gracilis nucleus.
Lateral inhibitory effects delimiting the area stimulated have also been described under the heading “surround” or “afferent inhibition” by Mountcastle (1957) and his co-workers. Thus Powell and Mountcastle (1959), recording from the somatic cortical area of the macaque monkey, have found skin fields in which a central nucleus of excitation to touch was surrounded by an inhibitory zone. The mechanism in this case may well be recurrent inhibition improving at each relay definition of locality.
Inhibition also apparently plays a decisive role in sharpening up information about quality. In some optic nerve fibers the spectral response in terms of threshold sensitivity appears restricted to, say, the red, green, or blue wave lengths. This is the so-called modulator type of response. The dominator type of response is sensitive across the spectrum. The modulator bands are now generally held to be caused by inhibition sharpening up color specification. Broad and narrow bands of spectral sensitivity have also been recorded from higher visual stations. A recent discussion of the neural mechanisms specifying wave length has been given by Granit (1962). As to specification of tonal quality, Galambos (1954) points out that inhibition in this system also restricts the originally broad sensitivity of the peripheral acoustic mechanism to a narrow band, a process that is likely to take place already within the cochlea. Tonal bands of different width, also depending upon the frequency range which the nerve fibers carry, are thus delivered to both the visual and the auditory cortical area.Centrifugal control
The sense organ in which centrifugal control is best understood is the muscle spindle; this organ is located within a spindle of thin muscles (so-called intrafusal muscle fibers) that are provided with special efferent fibers that can be stimulated both artificially and across natural reflex or supraspinal connections. Under such circumstances the intrafusal muscle fibers contract and thereby stretch the sensory spindle endings, which respond by discharging afferent impulses. There is a large literature in this field (Leksell 1945; Granit 1955) which cannot be reviewed here. Relevant in this connection is the principle of centripetal determination of the level of sensitivity in terms of spindle length. This is of fundamental importance because from the spindle the afferent impulses run to ventral horn cells, setting up efferent impulses to—among others—the large muscles in which the spindles are located; these muscles in turn are forced to contract until the tension on the sense organ is relieved. Thus, the length at which the muscle operates is determined by centrifugal control of spindle length, an interesting case of a centrally controlled sense organ which at the same time is a motor organ.
There is also a considerable literature on the olivo-cochlear Rasmussen bundle of efferent fibers, which exert a direct inhibitory effect that can be recorded both in auditory single fibers and at the cochlea. Both crossed and uncrossed olivo-cochlear fibers exert inhibitory effects, but their significance cannot yet be said to be fully understood. A possibility is that they play a role in binaural localization. (For the relevant literature see Galambos 1956; Fex 1963.)
The retina is likewise provided with centrifugal fibers, which is hardly surprising because it is a true nervous center in spite of its peripheral localization, and as pointed out above, centripetal control of nervous centers is common. The scant literature in this field has been summarized by Granit (1962).
At the level of detail alluded to in this brief review, analyses are restricted to the study of the organ of sight (see Hubel & Wiesel 1959; 1963; Jung & Kornhuber 1961). Hubel and Wiesel have made a thorough investigation of the receptive fields of cortical cells stimulating the eye (of a cat) by small visual objects influencing the firing of single cortical units. The receptive fields in the cortex were found to be organized either with excitatory onor inhibitory off-centers in the middle, the surrounds being of opposite character (see above for similarly organized retinal receptive fields). The cortical receptive fields are more elongated than the retinal ones, and they are oriented in different directions. The antagonism between center and periphery of the cortical receptive field makes stimuli covering the whole field or diffuse illumination relatively ineffective. The same properties make these fields extremely sensitive to form, size, position, and orientation of the stimulus and likewise sensitive to directional movement of a spot of light across the retina; this is easily understood, considering that a moving spot can traverse elongated fields in different directions. Some units were binocular, others monocular.
Recalling that Powell and Mountcastle (1959) had found that tactile cortical regions are columnar in shape with similar responses to a microelec-trode which apparently penetrates one of Ramόn’s sectors (see above) from above downward, Hubel and Wiesel (1963) made an analysis of receptive visual fields in a similar manner. They found a number of columns in the visual area in which receptive-field orientation was maintained, suggesting that columns of ordered sequences of field orientation are actually part of the central sensory mechanism, defined, of course, in functional terms.
[See alsoNervous System, articles on Structure And Function OF The BrainandElectroencephalography. Other relevant material may be found inHearing; Pain; Psychology, article onPhysiological Psychology; Skin Senses And Kinesthesis; Taste And Smell; Vision.]
Adrian, Edgar D. (1928) 1934 The Basis of Sensation: The Action of Sense Organs. London: Christophers.
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Granit, Ragnar; and Therman, P. O. 1935 Excitation and Inhibition in the Retina and in the Optic Nerve. Journal of Physiology 83:359–381.
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Hahtline, H. K.; and Ratliff, Floyd 1958 Spatial Summation of Inhibitory Influences in the Eye of Limulus, and the Mutual Interaction of Receptor Units. Journal of General Physiology 41:1049–1066.
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Jung, Richard; and Kornhuber, Hans (editors) 1961 Neurophysiologie und Psychophysik des visuellen Systems. The Visual System: Neurophysiology and Psychophysics. A symposium. Berlin: Springer. → Contributions in English, German, and French.
Kuffler, Stephen W. 1953 Discharge Patterns and Functional Organization of Mammalian Retina. Journal of Neurophysiology 16:37–68.
Lapohte, Y.; Lundberg, A.; and Oscarsson, O. 1956 Functional Organization of the Dorsal Spino-cerebellar Tract in the Cat. II: Single Fibre Recording in Flechsig’s Fasciculus on Electrical Stimulation of Various Peripheral Nerves. Acta physiologica scandinavica (Stockholm) 36:188–203.
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Starzl, T. E.; Taylor, C. W.; and Magoun, H. W. 1951 Collateral Afferent Excitation of Reticular Formation of Brain Stem. Journal of Neurophysiology 14:479–496.
Tunturi, Archie R. 1950 Physiological Determination of the Arrangement of the Afferent Connections to the Middle Ectosylvian Auditory Area in the Dog. American Journal of Physiology 162:489–502.
Woolsey, Clinton N. 1952 Patterns of Localization in Sensory and Motor Areas of the Cerebral Cortex. Pages 193–206 in Milbank Memorial Fund, The Biology of Mental Health and Disease. New York: Hoeber. → A discussion of Woolsey’s article appears on pages 206–225.
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