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CHEMOSENSORY PHYSIOLOGY

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IN AN AGE OF TRANSITION Vincent G. Dethier

Department of Zoology, University of Massachusetts, Amherst, Massachusetts 01003 In a recent published book entitled Masks of the Universe, the cosmologist Edward Harrison reminds us that we as a society create the universe in which we live and that each age fashions its own unique universe. Each of these universes is a mask of The Universe. Similarly, scientific verities are the creations of the society of contemporary scientists who believe as firmly as do cosmologists that their tenets represent reality. This reality changes with time. Each age tends to be but marginally charitable toward the "ignorance" of its predecessors and not especially sensitive to the possi­ bility that, as before, some of today's truths may become tomorrow's heresies. This is not to deny that shards of truth are salvagable from each age to the next; it is to remind us that comprehension at any time is profoundly influenced by contemporary intellectual ambience. Although historians of science can view from the mountain top of time the totality and comprehensiveness of the scientific endeavor and can discern the slow grandeur of its progress from one period to the next, the proximate eddies and currents that perturb the main stream are perhaps most acutely perceived by those who have lived through transitional periods. During a time of transition one is more deeply aware of the tenuous hold that science has on truth at any one moment, of the fragility as well as power of hypothesis and theory, of the influential role of improbabilities, and of the paradoxical relationship between concept and technology. The last point is particularly relevant in this time of high technology. Although new inventions and developments indubitably stimulate new ideas as well as provide means for solving old questions, the generation of ideas is not inextricably constrained by new technology. At most, realizations may be delayed. As Beidler (1987) has pointed out, 0147--006X/90/0301--0001$02.00

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technology cannot be substituted for keen insight, philosophical under­ standing, and serendipity. In some small measure the course of biology exemplifies the flux of conceptual cosmologies in general. Biology experienced a rapid transition from one age to another during the first three quarters of the present century. Classical biology was on the wane, molecular biology in the ascendancy, especially in the 1950s. In the 1960s, a new cohesive discipline began to emerge, neuroscience. I consider myself fortunate to have studied and practiced science during this period. It was a time of excitement, expectation, questioning, and discovery. It provided challenges, frus­ trations, and expanding vistas of terra incognita. In presenting this prefatory chapter I offer an account of my area of special interest, the chemical senses, as a vehicle to illustrate some general aspects of a period of transition, to record the importance of time, place, and informal eclectic personal interaction, to describe how ideas may develop, and to note their independence as well as their dependence on technology. Most especially I wish to present the thesis that cherishing a clear goal is essential but that at the same time one profits from peripheral vision. The "surround," to borrow a term from visual psychophysics, modulates and enriches the pursuit of a goal and ultimately places it in its clearest perspective. This essay, then, is not a review of the field. That has been done many times, the most recent being that of Finger & Silver (1987). It is a journey of inquiry through a period when electrophysiology was just coming of age and neuroscience had not yet emerged as a recog­ nized discipline. My early education in science began toward the end of the era of classical biology before any adumbrations of transition were apparent to the bio­ logical community as a whole. The starting point for me was a fascination with nature awakened by the beauty and vibrancy of living things, by sensual delight in colors, scents, sounds, and the cycling of the seasons, all enhanced by the inability of adults to answer satisfactorily the childhood "whys." Later, under the stern tutelage of formal science, the "whys" would become "whats" and "hows." The wonderment that sustained my interest in science throughout child­ hood and adolescence was almost obliterated during undergraduate days at Harvard. There, young aspiring biologists absorbed heavy doses of anatomy and taxonomy, preponderantly, of course, by examining pickled, mummified, and skeletonized specimens-or fossils thereof. At the very least, however, one learned the names of what was out there in the plant and animal world and approximately what each looked like externally and internally. Function, on the other hand, remained a mystery and was not related to behavior in any but the most obvious ways. Physiology, par-

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ticularly the machinery of the human body, flourished in the schools of medicine. Experimental zoology in this country and abroad was not held in high esteem in the first third of the century. A nodding acquaintance with physiology was acquired en route through two physiology courses. One course offered to our appetites was served up by Cannon, from whom I learned the "wisdom of the body" (1939). He also kept us informed about the controversy between the "electrical" people and the "purveyors of soup" over the nature of transmission at the neuromuscular junction. New discoveries about the role of acetylcholine, esserine, and ATP were only beginning to trickle into the curriculum. The pioneering work of Adrian on electrophysiology in the 1920s had not yet attracted wide attention (Adrian & Forbes 1922, Adrian 1926). None of this collegial enlightenment satisfied an eccentric interest that I had in the behavior of insects. The closest approach to animal behavior was provided by Welsh's course in invertebrate (mostly marine) physi­ ology. It did not offer any help toward solving questions in the area of my special interest, the obsessive gourmet habits of herbivorous insects. The only explanation of this gastronomic phenomenon extant postulated the existence of a "botanical" sense, a mysterious sixth sense. By analogy with my own eating habits, I suspected that chemical senses were involved. Although we students were constantly warned against the evil of anthro­ pomorphism, I learned over the years that there was considerable heuristic value in posing questions from this point of view. At Harvard in the 1930s there were two specialists in the field of chemo­ reception, Parker and Crozier. Neither was currently active in that field, having turned to other matters, but each had written reviews (Parker 1922, Crozier 1934) that summed up knowledge about these least understood of all sensory systems. At this time, knowledge of the chemical senses was restricted to anatomy and histology as constrained by limits of the light microscope and gross anatomy. Only gold and silver impregnation and methylene blue staining were available for revealing the tracery of the nervous system. Generally speaking, investigators were focusing their attention on gross anatomy, histology, thresholds, classification of tastes and odors, relations of sensation to chemical structure, theories of action, psychophysics, flavor, and perfumery. The emphasis throughout lay on vertebrates. Insofar as insects were concerned, zoologists occupied themselves in free speculation. Despite a great legacy of elegant nineteenth century histology, there was no unanimity of opinion regarding the loci of chemosensory organs, no consensus as to whether there were separate and distinct olfac­ tory and gustatory senses, and no knowledge concerning the identity of the end-organs themselves.

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If the problem of insect monophagy was to be solved, the identity and response characteristics of the chemoreceptors had to be revealed. The first and only conceivable approach was to combine ablation, anesthesia, and occlusion of putative end-organs with behavioral observations. By means of these techniques tentative identification of some olfactory organs, among them those of caterpillars, was made during the period 1921-1941 (von Frisch 1921, Dethier 1937, 1941). A new approach was needed. Although I had acquired a vicarious acquaintance with the pioneering technique of electrophysiology of the 1920s by reading Adrian's Basis of Sensation (1928), I had neither the knowledge nor the equipment to apply this new approach to my problem. The instruments that existed were the Einthoven string galvanometer, the Lippmann capillary electrometer, and the Matthews oscillograph. They were available in a few laboratories only, notably Adrian's in Cambridge, Forbes' at Harvard, and Erlanger's and Gasser's at Washington University. Most investigators using this equipment were concerned with trying to understand the nature of the action potential (Gasser & Newcomer 1921, Gasser & Erlanger 1922). Motor nerves and the sensory nerves of mechanoreceptors were the prep­ arations best suited for this research. Only a few attempts to record from chemosensory nerves were made in the early 1930s. Hoagland (1933) detected but could not resolve electrical activity in nerves of the lips and barbels of catfish in response to salt and acid; Zotterman (1935) recorded impulses in the chorda tympani and glossopharyngeal of the rat; Pumphrey (1935) recorded responses to salt and acid placed on the tongue of the frog; Adrian & Ludwig (1938) recorded activity in the olfactory nerves of catfish and carp. At this time, through chance encounters, I made the acquaintance of Roeder at Tufts College and Prosser at Clark University. Roeder had arrived at Tufts in 1932 and Prosser at Clark in 1934. Roeder's entree to electrophysiology came as a consequence of his taking a course at Woods Hole, where Prosser was instructing. Prosser was investigating electrical activity in the nerve cord of earthworms and marine invertebrates by means of a Matthews oscillograph and amplifier. Roeder applied this technique together with ablation to studies of copulatory behavior in praying mantids. At Prosser's invitation I spent part of one summer at Clark, where we attempted to record from chemosensory nerves of caterpillars. Activity from mechanoreceptors was detected, but only physiological silence and instrumental noise followed chemical stimulation. Attempts continued intermittently and unsuccessfully until the advent of World War II. In the meantime Roeder, a skilled and ingenious tinkerer, was perfecting his instrumentation and techniques for recording from the central nerve

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cord of the cockroach. Shortly after the war, he and I made another attempt to record from chemoreceptors. Having observed that the very long ovipositors of some parasitic wasps were sensitive to chemical stimu­ lation, I thought that the correspondingly long sensory nerve might lend itself to recording. Again we failed to detect any action potentials. At this point behavior seemed to offer a more promising approach to the problems of chemoreception. The turning point came as the result of two lucky decisions, namely, that the caterpillar was not the most coop­ erative animal and that gustation was more tractable than olfaction. The choice of the blowfly was serendipitous. In 1922 Minnich had observed that flies and butterflies extended their proboscises when the legs were touched with sugar. Four years later he reported in one short sentence that touching a single long curved hair on the proboscis of the blowfly with sugar elicited extension (Minnich 1926). Here was a preparation where single chemoreceptors could be isolated and gustation studied behaviorally without the usual confounding postingestional effects. Early in 1953, a student, Grabowski, and I succeeded by microtopical application of sucrose to single hairs in demonstrating unequivocally that the gustatory end-organs of the tarsi were hairs (setae) similar in appear­ ance to those on the labellum, which Minnich had identified as gustatory (Grabowski & Dethier 1954). We were able to prove that the tips were not covered with cuticle, that the hairs were innervated by three bipolar sensory neurons (later examination with an electron microscope revealed two additional neurons), and that each of the cells responded to a different sensory modality. It was immediately apparent that this preparation could serve as an excellent model of a gustatory apparatus because, unlike the vertebrate taste papillae, the receptors were primary neurons, the axons of which led directly without synapsing into the head ganglia. During the next ten years it was possible with this preparation to examine the response spectra of the chemosensory cells, detail, separate, and mea­ sure peripheral and central adaptation, measure temporal and spatial summation, evaluate differential thresholds (AI/I), relate responsiveness to the structural configuration of stimulating molecules, propose a pro­ visional functional map of gustatory projections in the central nervous system, demonstrate and evaluate in an intact organism central excitatory and inhibitory states as Sherrington had done with the flexion reflex in spinal cats, advance promising hypotheses regarding the nature of molec­ ular receptor sites and transduction, and lay a groundwork for elucidating mechanisms underlying hunger and satiation. All of this work was eventu­ ally summarized in the book, The Hungry Fly (Dethier 1976). The goal throughout this period was to understand the neural mech­ anisms mediating chemosensory responses and related behavior. At the

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same time, it was the behavior that was providing insight to the mechan­ isms. The behavioral approach was an exciting game of wits. It proved to be a powerful tactic, and many of its findings were subsequently shown by electrophysiology to be gratifyingly accurate. Through the period of the late 1940s to 1958 there had been no break­ through in the impasse to successful electrophysiological recording from insect chemoreceptors. Investigation of vertebrate systems had been making considerable progress, as exemplified by Pfaffmann's beautiful recordings of single chorda tympani fiber responses in the cat. At the Johns Hopkins University, to which I had moved after the war, Bronk, Hartline and others of the group were fully engaged in electrophysiologi­ cal work; however, the only experimentation in chemoreception was being conducted by Beidler (then a graduate student). He was studying the integrated response of multiple chorda tympani fibers of the rat. Most of the studies with vertebrates were concerned with the neural basis of the four classical taste modalities. In Europe there was progress in the field of olfaction, beginning with Adrian & Ludwig's (1938) recording of electrical activity in the olfac­ tory nerves of catfish and carp and Adrian's (1942) recording of activity in the olfactory projections in the brain of the hedgehog. In 1953, Boiste1 and Coraboeuf succeeded in recording mixed neural responses in insect antennae. It was Schneider in Germany, however, who finally made a breakthrough (1955). Realizing in 1952-1953 that in thc silkworm moth's response to specific pheromones he had the perfect experimental animal and thc perfect olfactory stimulus, he exploited that system fully and in 1955 recorded the first single unit olfactory responses to pheromones. This accomplishment paved the way for his own elegant work and that of Kaissling, Boeckh, and others (Boeckh, Kaissling & Schneider 1965). The insect gustatory system remained intransigent, but behavioral analysis continued. In thc course of measuring behavioral thresholds, a number of workers observed that sensitivity decreased as the duration of deprivation increased. The question of whether the sensitivity of the receptors them­ selves changed or some postingestional factors influenced response steered our research in a direction that was also being investigated in vertebrates. Physiologists and physiological psychologists were probing the central nervous system for answers. Hetherington & Ranson (1942) had dis­ covered that hypothalamic lesions in the brain of the rat affected feeding. Anand & Brobeck (1951a,b) at Yale and Teitlebaum & Stellar (1954) at Hopkins were also lesioning the brain. At that time it was believed that the lateral hypothalamus was a hunger or feeding center and the ventromedial hypothalamus a satiety center. In time the mechanisms were discovered to

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be more complex. Eventually, in the years to follow, investigators of the vertebrate system gradually worked their way toward the periphery, while those of us studying the blowfly were working from the periphery inwards. Still employing threshold as a monitor, my associates and I began to isolate by surgery, ligation, and intubation various parts of the digestive system as possible origins of signals modulating the response to chemo­ sensory stimulation. Complementary tests involved injection of the haemo­ cole and also parabiosis. One tremendous advantage of the fly over the rat was the possibility of removing the entire digestive tract together with the oral gustatory receptors and a bit of brain and studying ingestion in vitro. Thus, by a process of elimination we determined that one mechanism regulating behavioral threshold and therefore ingestion was resident in the stomatogastric system, the analogue of the vertebrate autonomic system. At this point in the investigation I discussed the problem with Dietrich Bodenstein, who was then a civilian employee at the Army Chemical Center in Edgewood, Maryland. Bodenstein was a developmental biologist who worked both on amphibians and cockroaches. He was one of the pioneers in insect developmental biology and a superb microsurgeon. When I mentioned to him my plan to section the recurrent nerve, he assured me that the operation was simplicity itself and proceeded to demonstrate by operating successfully on some Drosophila. Following his technique I sectioned the nerve in blowflies; the result was spectacular, a rapid and extreme hyperphagia. The whole sequence of normal feeding then became explicable in terms of interaction between chemosensory excitation and central inhibition triggered by internal mechanoreceptors (Dethier & Bodenstein 1958). This work, together with elaboration in the 1960s by Gelperin (l966a,b, 1967) and more recent refinements in our laboratory, gave us one of the most complete pictures of neural mechanisms of feed­ ing up to that time. In 1957 I was able to return to the gustatory receptor itself because of a remarkable innovation in electrophysiological recording. Hodgson, who had left our laboratory to continue postdoctoral studies with Roeder, developed, together with Lettvin and Roeder (1955), a technique that solved the problem of recording from single chemosensory sensilla. By one of those odd coincidences of science, Morita and his associates at Kyushu University made the same discovery in 1957. A glass micropipette con­ taining weak saline plus the stimulating compound to be tested was placed over the tip of the hair and served as a salt bridge to a Ag/AgCl wire. Shortly thereafter Morita (1959) developed an elegant refinement whereby he inserted an electrode through a hole drilled in the shaft of the hair. At Hopkins, Wolbarsht, Evans, and I immediately applied these new techniques to studies of the sensitivity and action spectra of individual

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chemosensory cells. The early behavioral conclusion that there was a sugar-sensitive cell, a salt-sensitive cell, and a mechanoreceptor was confirmed. In addition, the existence of two other cells, a water receptor (Wolbarsht 1957) and a second but distinctive salt receptor, was revealed. The first electron microscopic studies by Larsen (1962) in our labora­ tory and Adams et al (1965) at Rutgers University confirmed the existence of these cells, thus correcting the early methylene blue evidence. These technical developments now made possible pursuit of two prob­ lems that had constituted the crux of chemosensory physiology from the beginning, namely transduction and coding. A chance observation by Barnhard & Chadwick at the Army Chemical Center in 1953 had put us on the track. They had observed that bait frequented by flies was more attractive than bait that had been protected from visiting flies. The obvious reason seemed to be that regurgitation and defecation altered the material; however, flies with both proboscis and anus plugged also enhanced the attractiveness. On a hunch I eluted the legs of flies with water, added sucrose to the eluate, and tested for enzyme activity. The eluate contained an alpha-glucosidase. The idea that this enzyme might initiate the process of transduction was tempting; however, since it was already known that some sugars without alpha-glucosidase linkages and some pentoses and hexoses as well were adequate stimuli, we did not pursue the matter further. Hansen in Germany and Morita, Kijima, Koizumi, and their associates in Japan picked up the trial (Hansen & Kuhner 1972, Kijima et al 1973). They proved that the enzymes were intimately and exclusively associated with the receptors. Exactly what part the glucosidases play in the process of transduction is still a mystery. The relation between the sensitivity of the sugar receptor and the con­ figuration of carbohydrate molecules was also unknown. Neither von Frisch (1935) nor I (1955) had been able to make any sense of the com­ parative stimulatory effectiveness of the various sugars. The first clue appeared in 1955, when behavioral studies of mixtures revealed that some sugars synergized and others inhibited each other. Evans (1963) suggested that the sugar receptor cell contained multiple molecular sites, specifically one for pyranose and one for furanose sugars [the idea of different multiple sites had been proposed earlier by Biedler for the rat salt receptor (1957, 1962)]. Six years later electrophysiological support for this hypothesis was provided (Omand & Dethier 1969). The matter was finally settled by Morita & Shiraishi (1968) and Shimada et al (1974) by further electro­ physiological and pharmacological studies. As the matter now stands, the sugar receptor of the blowfly is presumed to have four specific molec­ ular sites. Comparable studies of the nature of the salt receptor were stimulated

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by Beidler's work at Hopkins with the rat chorda tympani. His equation based on the Law of Mass Action was found by Evans & Mellon (1962) to apply to the salt receptor of the fly. One remaining series of studies attempting to relate stimulating effec­ tiveness and chemical structure is worth mentioning. Over the years, begin­ ning in 1947, more than 200 aliphatic compounds were tested and found to cause flies to reject sugar solutions. It was believed that these compounds stimulated a receptor mediating rejection. The "rejection" threshold could be predicted with great accuracy from the structural formulae. Discussions with Brink at Hopkins prompted me to apply to these data the same thermodynamic analyses that he and Posternak had made of narcotics (Brink & Posternak 1948). It was not until later (1965) in our laboratory at the University of Pennsylvania that Hanson showed electrophysiologically that these aliphatic compounds, rather than stimulating a "rejection" receptor, were narcotizing the receptors mediating acceptance. Steinhardt et al (1966) came to a similar conclusion. Despite these forays into the nature of transduction, the bearing of gustation on feeding continued to be a central theme in our work. Richter, at the peak of his studies of food preference by the rat and the relation between preference and nutritional need, often visited our laboratory and observed a "two-bottle" preference apparatus that a student (Rhoades) and I had designed in emulation of his apparatus for rats (Dethier & Rhoades 1954). He encouraged us to investigate long-term ingestion and preference as they related to nutrition. Seven years earlier at the Army Chemical Center, a comprehensive survey of the nutritional adequacy of various carbohydrates had been undertaken (Hassett, Dethier & Gans 1950), so the stage was set for a study of preference. The final results indicated that insofar as sugars were concerned, taste preference was not an infallible guide to nutritional value. After eleven stimulating and productive years at Hopkins, where I learned electrophysiology, electron microscopy, and physiological psy­ chology, I moved to the University of Pennsylvania, where there was a strong multidisciplinary group studying many and varied aspects of feeding behavior at the Institute of Neurological Science. There the lines of work already described were continued and expanded. Another set of gustatory receptors was discovered in the oral cavity of flies; the sensory basis of water, alcohol, and protein ingestion was investigated, and the existence and characteristics of central excitatory and inhibitory states initiated by chemosensory input were established. Advances in our knowledge of the chemoreceptors of the fly and the evolution of modern techniques prompted a return to the investigations on caterpillars begun 30 years earlier. Caterpillar gustatory receptors were

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discovered to be more complicated and versatile than those of the blowfly. They also appeared to be less specific, more broadly tuned. Schneider had classified the olfactory receptors of the silkworm moth as "specialists" and "generalists." The receptors of caterpillars fell somewhere between these two extremes of a response spectrum. Extensive recording of responses to plant saps led to the hypothesis that differential preferences were mediated by patterns of impulses from multiple receptors. Explanations previous to this, molded by Verschaffelt's (1910) discovery that special compounds triggered feeding and by the prevailing ethological concept of "sign" stim­ uli, emphasized the specificity of receptors. A theory stressing the import­ ance of multineuronal afferent patterns (across-fiber patterns) proposed by Pfaffmann (1941) and eloborated by him and by Erickson (1963) seemed to fit the case of caterpillars. This work continued for many years at Pennsylvania and then at Princeton. Eventually some progress was made in decoding chemosensory messages with the help of information theory and analysis of spike-interval distributions by autocorrelograms ( Dethier & Crnjar 1982). The investigative journey in this selected field of inquiry has come full circle in the period spanning the very early development of neuro­ physiology in the first third of the century to the sophisticated arma­ mentarium of neuroscience of the present. The character of the pursuit of knowledge in the field of chemoreception and related behavior reflects the general nature and evolution of sensory physiological investigation in this period of transition. The enlistment of ingenuity and indirect approaches that characterized general physiology in the 1920s when direct approaches were technically impossible carried sensory physiology forward. Aware­ ness of progress in apparently unrelated fields facilitated advance toward focused goals. A contrapuntal relation gradually developed between ideation and technology. In the broad search for and understanding of behavior, the investigation had advanced contripetally from sense organs to central phenomena, from a proximate goal of understanding the mechanics of stimulation at the receptor level to decoding sensory spike trains. Furthermore, it moved from information transmission to the meaning of all this for behavior. I do not presume to imply that all the questions addressed had been answered. It is clear, however, that what began as a specialized, one might even say parochial, interest, expanded along the way to contribute some measure of insight to broader issues relating neural machinery to behavior. At the beginning of this prefatory chapter! referred to Harrison's Masks of the Universe. In introducing universes that are impermanent cosmic belief-systems of societies, he alluded also to private world pictures. Among the data from which these private worlds are constructed are sensory data.

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Though our perception of the world changes with our intellectual and introspective knowledge, it still is limited by our senses. Considering that advanced technologies enormously extend our senses, one might well wonder whether biologically evolved sensory systems any longer faith­ fully serve our needs. To what extent does the world as perceived directly by sense organs have reality and validity? The molecular and time/space world, which we are convinced exists, is obviously different from the biological world as perceived. The perceived world of infrahuman animals is certainly a reality in that, insofar as they survive and evolve successfully in the physical world, they perceive it correctly and so attest its reality. We, on the other hand, can generate our own perceptions independently of what our sense organs tell us. When we know that there is a Chernobyl, we act as though we can indeed sense it (even without the benefit of aversion-learning). Paramount though the mind/brain problem may be for understanding behavior, the brain is limited in its perfection by sensory input, even though it can stimulate itself by introspection. Studies on sensory deprivation prove the need for sensory input (Zubek 1969). Thus, sensory physiology contributes in a major way to human understanding. Sense organs provide our only direct contact with the universe. Granit (1955) touched the heart of the matter when he wrote that sensory physiology is "a branch of natural science which is actually capable of giving some meaning to 'meaning'. " Literature Cited Adams, 1. R., Holbert, P. E., Forgash, A. J. 1965. Electronmicroscopy of the con­ tact chemoreceptors of the stable fly, Stomoxys, calcitrans (Diptera: Muscidae). Ann. Ent. Soc. Amer. 58: 909-17 Adrian, E. D. 1926. The impulses produced by sensory nerve endings. Part I. J. Physiol. 61: 49-72 Adrian, E. D. 1928. The Basis of Sensation: The Action of the Sense Organs. London: Christophers Adrian, E. D. 1942. Olfactory reactions in the brain of the hedgehog. J. Physiol. 100: 459-73 Adrian, E. D., Forbes, A. 1922. The all-or­ nothing response of sensory nerve fibers. J. Physiol. 56: 301-30 Adrian, E. D., Ludwig, C. 1938. Nervous discharges from the olfactory organs of fish. J. Physiol. 94: 441--60 Adrian, E. D., Zotterman, Y. 1926. The impulses produced by sensory nerve end­ ings. Part 2. The response of a single end­ organ. J. Physiol. 61; 151-71

Anand, B. K., Brobeck, J. R. 1951a. Hypo­ thalamic control of food intake in rats and cats. Yale J. BioI. Med. 24: 123-40 Anand, B. K., Brobeck, J. R. 1951b. Local­ ization of a "feeding center" in the hypo­ thalamus of the rat. Proc. Soc. Exp. BioI. NY 1951: 323. Barnhard, C. S., Chadwick, L. E. 1953. A "fly factor" in intractant studies. Science 117: 104-5 Beidler, L. M. 1954. A theory of taste stimu­ lation. J. Gen. Physiol. 38: 133-39 Biedler, L. M. 1957. Physiological basis of taste psychophysics. Fed. Proc. 16; 9 Beidler, L. M. 1962. Taste receptor stimu­ lation. In Progress in Biophysics and Biophysical Chemistry, ed. J. A. V. Butler, H. E. Huxley, R. E. Zirkle, 12; 107-51. Oxford: Pergamon Beidler, L. M. 1987. Research directions in the chemical senses. In Neurobiology of Taste and Smell, ed. T. E. Finger, W. L. Silver, pp. 423-37. New York: Wiley Boeckh, J., Kaissling, K. E., Schneider, D.

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1965. Insect olfactory receptors. Cold Spring Harbor Symp. Quant. Bioi. 30: 263-80 Boiste!, J., Coraboeuf, E. 1953. L'activite electrique dans l'antenne isolee de Lepi­ doptere au cours de i'etude de i'olfaction. CR Soc. BioI. Paris 147: 1172-75 Brink, F., Posternak, J. M. 1948. Thermo­ dynamic analyses of the relative effec­ tiveness of narcotics. J. Cell Compo Physiol. 32: 211-33 Cannon, W. B. 1939. The Wisdom of the Body. New York: Norton Crozier, W. J. 1934. Chemoreception. In A Handbook of Experimental Psychology, ed. C. Murchison, pp. 987-1036. Worces­ ter, Mass.: Clark Univ. Press Dethier, V. G. 1937. Gustation and olfaction in lcpidoptcrous larvae. BioI. Bull. 72: 723 Dethier, V. G. 1941. The function of the an­ tennal receptors in lepidopterous larvae. BioI. Bull. 80: 403-14 Dethier, V. G. 1955. The physiology and histology of the contact chemoreceptors of the blowfly. Q. Rev. bioi. 30: 348-71 Dethier, V. G. 1976. The Hungry Fly. Cam­ bridge: Harvard Univ. Press Dethier, V. G., Bodenstein, D. 1958. Hunger in the blowfly. Z. Tierpsychol. 15: 129-40 Dethier, V. G., Crnjar, R. M. 1982. Can­ didate codes in the gustatory system of caterpillars. J. Gen. Physiol. 79: 549-69 Dethier, V. G., Rhoades, M. V. 1954. Sugar prefer ence aversio n functions for the blowfly. J. Exp. Zool. 126: 177-204 Erickson, R. P. 1963. Sensory neural pat­ terns and gustation. In Olfaction and Taste, ed. Y. Zotterman, 1: 205-13. Oxford: Pergamon Evans, D. R. 1963. Chemical structure and stimulation by carbohydrates. In Olfac­ tion and Taste, ed. Y. Zotterman, I: 16592. Oxford: Pergamon Evans, D. R., Mellon, DeF. 1962. Stimu­ lation of a primary taste receptor by salts. J. Gen. Physiol. 4: 651 61 Finger, T. E., Silver, W. L. 1987. Neuro­ biology of Taste and Small. New York: Wiley Gasser, H. A., E rlanger, J. 1922. A study of t he action currents of nerve with the cathode ray oscillograph. Am. J. Physiol. 62:496-524 Gasser, H. S., Newcomer, H. S. 1921. Physiological action currents in the phrenic nerve. An application of the thermionic vacuum tube to nerve phys­ iology. Am. J. Physiol. 57: 1 26 Gelperin, A. 1966a. Control of crop empty­ ing in the blowfly. J. Insect Physiol. 12: 331-45 Gelperin, A. 1966b. Investigation of a fore-

gut receptor essential to taste threshold regulation in the blowfly. J. Insect Physiol. 12: 829-41 Gelperin, A. 1967. Stretch receptors in the foregut of the blowfly. Science 157: 20810 Grabowski, C. T., Dethier, V. G. 1954. The structure of the tarsal chemoreeeptors of the blowfly, Phormia regina Meigen. J. Morph. 94: 1-17 Granit, R. 1955. Receptors and Sensory Per­ ception. New Haven: Yale Univ. Press Hansen, K. 1968. Untersuchungen iiber den Mechanismus der Zucker-Perzeption bei Fliegen. Habilitationschrift der Universi­ tat Heidelberg Hansen, K., Kuhn er, 1. 1972. Properties of a possible receptor protein of the fly's sugar receptor. In Olfaction and Taste IV, ed. D. Schneider, pp. 350-56. Stutt­ gart: Wissenshaftliche Verlagsgesellschaft MBM Hanson, F. E. 1965. Electrophysiological studies on chemoreceptors of the blowfly, Phormia regina Meigen. Phd dissertation, Univ. Penna., Philadelphia Harrison, E. 1985. Masks of the Universe. New York: Macmillan Hassett, C. C., Dethier, V. G., Gans, J. 1950. A comparison of nutritive value and taste thresholds of carbohydrate for the blow­ fly. BioI. Bull. 99: 446-53 Hetherington, A. W., Ranson, S. W. 1942. The spontaneous activity and food intake of rats with hypothalamic lesions. Am. J. Physiol. 136: 609-17 Hoagland, H. 1933. Specific nerve impulses from gustatory and tactile receptors in cat­ fish. J. Gen. Physiol. 16: 685-714 Hodgson, E. S., Lettvin, J. Y., Roeder, K. D. 1955. Physiology of a primary chemoreceptor unit. Science 122: 417-18 Kijima, H., Koizumi, 0., Morita, H. 1973. IX-Glucosidase at the tip of the contact chemosensory seta of the blowfly, Phormia regina. J. Insect Physiol. 19: 1351-62 Larsen, J. R. 1962. The fine structure of the labellar chemosensory hairs of the blow­ fly, Phormia regina Meigen. J. Insect Phy­ siol. 8: 683-91 Minnich, D. E. 1922. The chemical sen­ sitivity of the tarsi of the red admiral butterfly, Pyrameis atalanta Linn. J. Exp. Zool. 35: 57-81 Minnich, D. E. 1926. The organs of taste on the proboscis of the blowfly, Phormia regina Meigen. Anat. Rec. 34: 126 Morita, H. 1959. Initiation of spike poten­ tials in contact chemosensory hairs of insects. III. D.C. stimulation and genera­ tor potential of labellar chemoreceptor of Calliphora. J. Cell. Compo Physiol. 54: 182-204

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Morita, H. 1974. Separation of two recep­ tor sites in a single labellar sugar receptor of the flesh-fly by treatment with p-chlo­ romercuribenzoate. J. Insect Physiol. 20: 605-21 Steinhardt, R. A., Morita, H., Hodgson, E. S. 1966. Mode of action of straight chain hydrocarbons on primary chemo­ receptors of the blowfly. Phormia regina. J. Cell. Physiol. 67: 53-62 Teitlebaum, P., Stellar, E. 1954. Recovery from failure to eat produced by hypo­ thalamic lesions. Science 120: 894-95 Verschaffelt, E. 1910. The cause determining the selection of food in some herbivorous insects. Proc. R. Acad. Amsterdam 13: 536-42 von Frisch,. K. 1921. Uber den Sitz des Geruchsinnes bei Insekten. Zool. Jahrb. Abt. Zool. Physiol. 38: 449-516 von Frisch, K. 1935. Uber den Geschmacks­ sinn der Bi_me. Z. Physiol. 21: 1-156 Wolbarsht, M. L. 1957. Water taste in Phor­ mia. Science 125: 1248 Zotterman, Y. 1935. Action potentials from the chorda tympani. Skand. Arch. Physiol. 72: 73-77 Zubek, J. P. 1969. Sensory Deprivation: Fifteen Years of Research. New York: Appelton-Century-Crofts

Chemosensory physiology in an age of transition.

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