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DO BAJA

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SUSUMU HAGIWARA November 6, I 922-Apri;t I, ~ 989 BY THEODORE H. BULLOCK AND ALAN D. GRINNELL BORN IN BARE, Hokkaido, Japan, on November 6, 1922, the son of a school principal, Susumu Hagiwara went through public schools, graduating from high school in Mito, Honshu. Among the boyhooc! hobbies that persistec! through- out his life were butterfly observation en c! collecting, be- gun with his father. He also enjoyoc! birc! watching en c! painting. He was one of the select few admitted to the pres- tigious University of Tokyo. There he completec! both his medical degree in 1946 and Ph.D. in physiology under Prof. T. Wakabayashi in 1951. During this perioc! he was cliag- nosec! with tuberculosis en c! hac! one lung removed, but he continues! to write papers cluring his convalescence en c! recovered enough to live a surprisingly normal life. In 1948 his first paper clemonstratec! that cicadas begin to sing at a certain level of light in the morning, clelayoc! corresponclingly on cloucly clays. His thesis topic, the fluc- tuation of intervals in rhythmic excitation in frog stretch receptors, with comparisons to the intervals in human mo- tor units cluring voluntary movement, foretoIc! a lifelong bent towarc! comparative physiology. AIreacly prolific, he publisher! a substantial series of papers before 1953 on top- ics as diverse as the myogenic rhythm in cicada muscles (with A. Watanabe), the first penetration of Mauthner's neu 59

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60 BIOGRAPHICAL MEMOIRS ron in fish (with I. Tasaki en c! A. Watanabe), en c! the statis- tical analysis of neuronal firing intervals. Each was a pio- neering contribution, the last mentionec! is often cites! as a seminal stucly in the fielc! now caller! neural computation that is rising rapicIly in parallel with molecular neurobiol- ogy, the one more system oriented, the other more recluc- tionist. Susumu Hagiwara cannot be pigeon-holec! in one camp or the other. One of the fascinations of this man's career is that a true hero of general physiology owes the essence of his fame to comparative studies, not in the usual sense that he spent his life on an unconventional favorable species but in sam- pling many species, far apart phylogenetically, upward of sixty different preparations in about as many species, from plants to humans, from clonal pituitary cells to leech neu- rons, from cicadas to barnacles, giant squid to bats, chirp- ing bircis to clam larvae, soft corals to mouse hybricloma cells, invertebrate eggs to cats. The motivation to search cleliberately for unusual materials en c! to explore the woric! of species is an obvious threat! throughout his work en c! more than a leitmotif. He learner! early the lesson that even so basic an organelle as the cell membrane cannot be represented adequately by any one exemplar. He set out to broaclen our view of nature's scope en c! range of available mechanisms. Pretending to know nothing about zoology or botany, he asker! his friends in that gentle, unclemancling manner: "What kincis of eggs can we get? Where can one get amphioxus? Where is an example of a distributed synapse?" (The an- swer to the last is the sabellic! polychaete giant, which he then took for stucly.) "If it's not too much trouble, is there any chance we could get some hummingbirds?" Procure- ment problems were a constant source of amazement en c! amusement. Susumu's antennae were tuned to the first hint

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SUSUMU HAGIWARA 61 of interesting material, as when Graham Hoyle cliscoverec! the giant muscle fibers in a North Pacific barnacle en c! later the simple photoreceptors in barnacles. Fincling him- self on the Great Barrier Reef or the Amazon River, Hagi couIc! quickly fins! a remarkable species en c! bit of tissue in that species. To be sure, some preparations were suggestec! to him, but the notable feature was the instant sympathetic response en c! eagerness to try his iriclectomy scissors en c! skillful fingers on it. Some preparations were not so cleli- cate. It requires! 75-mm nails hammerer! into a hardwood! plank to hoIc! clown a strong electric eel or Gymnarchus, both of which jerk each time they inclulge in an air-breath- ing gulp. If it needed another example, Hagiwara's life outstand- ingly illustrates! how fincling differences among species, prepa- rations, or cell types can be a major source of insight into general physiology. This premier intracellular biophysicist must also be recognizes! as a neuroethologist. Not only is this true because of the implicit relevance of his membrane discoveries to species-characteristic behavior, but he was ex- plicitly interested! in uncovering the mechanisms of out- stancling examples of natural behavior. How floes a cicada sing? How does a hummingbird move its wings? What rules apply to interval distribution in a chirping bircl's rhythm or the intervals between gulps in air-breathing loaches in the aquarium besicle his hospital becI? These examples mani- fest his lifelong interest in animals as such. At the time Hagiwara completed his Ph.D., Yasuji Katsuki (1905-94), heat! of the Department of Physiology of the Tokyo Medical and Dental University, was building a group that became the most fertile laboratory in sensory neuro- physiology in the country. He was an international figure in auditory physiology who appreciates! en c! himself inclulgec! in many comparative studies, among diverse animals and

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62 B I O G RA P H I C A L EMOIRS various mociaTities. He recruitec! Hagiwara to his clepart- ment in 1950 as his seconc! in commanc! en c! soon clepartec! for a two-year stint abroad, inclucling working periods in the laboratory of one of the authors (T.H.B.~. During this early perioc! at the TMDU, Hagiwara completec! a series of studies on (~) the curious sonic muscle in certain cicadas that produce their summer buzzing sounc! by a myogenic rhythm, (2) the neuromuscular transmission in insects, (3) intracellular recording in Mauthner's neuron in catfish en c! insect muscle, en c! (4) a prescient paper on the effects of tetraethylammonium chIoricle on the muscle cell membrane. When Katsuki returned, he promptly sent Hagiwara abroac! for a similar two-year sequence of working visits to laborato- ries in Europe en c! the Uniter! States. Hagi spent such a period with Yngve Zotterman in Stockholm, participating in recording from the chorcia tympani nerve of cats. He visited Sven Dijkgraaf in Utrecht, John Pringle, Alan Hodgkin, en c! Lorc! Adrian in Cambridge, en c! Ichiji Tasaki in Bethesda, MarylancI. After six month at UCLA en c! three months at the Marine Biological Laboratory in Woocis Hole with T.H.B. Hagiwara spent several months at the Johns Hopkins Uni- versity working with Charles Ec~warcis en c! Stephen Ruffler, several months in New York at Rockefeller University, en c! half a year at the National Institute of Neurological Dis- eases en c! Blinciness in Bethesda with Tasaki. All this re- sultec! in experience en c! papers on the physiology of taste in cats, cardiac ganglion pattern generators in lobsters, gi- ant synapses in squid, stretch receptors in crayfish, en c! the electrical capacitance of muscle fiber membranes, among others. He returnee! to Japan in 1957 en c! within two years rose to professor in the Seconc! Department of Physiology in the Tokyo Meclical en c! Dental University. He soon cliscoverec! that the expectations en c! obligation in this role were not

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SUSUMU HAGIWARA 63 for him and his chronic lung problem. He rejoined Bullock in Los Angeles in 1960 en c! by 1964 became completely inclepenclent, with his own laboratory en c! grants. During these years, while Hagi rapidity rose to the rank of research professor, eventually to overscale professor, we enjoyoc! many joint projects. Some brought clistinguishec! Europeans such as LaclisTav Tauc, Thomas Szabo, Hans Lissmann, en c! Per Enger, as well as accomplishes! en c! promising co-workers from Japan, inclucling Hiromichi Morita, Koroku Negishi, Kenichi Naka, Shiko Chichibu, en c! Nobuo Suga. Besicles continuing with previous preparations, Hagi en c! his co-work- ers began experiments on electroreceptors, polychaete gi- ant synapses, en c! barnacle en c! hummingbirc! muscle. It was still possible to maintain active interest in both integra- tive en c! ion channel mechanisms, much to the benefit of both fielcis. Hagi traveler! flaring these years, visiting, for example, Hans Lissman in camor~c~ge, Attract t-essarct In parts, anct Angelique Arvanitaki in Monaco. From a hospital in Rome ~. . ~. ~. , O. he wrote: "I was brought to this hospital unconscious from the hotel . . . acute pneumonia . . I lost all my weight. Since I clic! not have much weight, I am almost losing myself." He flew to Tokyo to recuperate, surprising his family and miss- ing his symposium. This was not the first or the last episode of health problems cluring his trips, but it is significant that .. ... . . . . ~. , . O tney cocci not stop norm trom traveling even to fairly remote places. One notable trip was in March 1964 to the U.S.-lapan Joint Cooperative Program Symposium on Neurophysiology, for which the Japanese clelegation, lee! by Yasuji Katsuki, incluclec! Tasunosuke Araki, Taro Furukawa, Kojiro Matsucia, Koichi Motokawa, Yutaka Omura, Masayasu Sato, Sadataka Takagi, Tsuneo Tomita, Koji Uchizono, en c! Akira Watanabe. The U.S. clelegation, lee! by T. H. Bullock, incluclec! Michael

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64 B I O G RA P H I C A L EMOIRS Bennett, Robert Galambos, Harry Gruncifest, Susumu Hagiwara, CarIton Hunt, Stephen Ruffler, Davic! Potter, Floyc! Ratliff, en c! Walter Rosenblith. We mention the names be- cause this influential meeting triggerec! a number of later projects en c! collaborations. We recall the visit Hagi, Mike Bennett, en c! Bullock macle together, after the symposium, to the beautiful seaside resort of Shirahama. They asker! the attendant in the public bath why it happened that they were the only bathers en c! were toIc! that they were the only guests who were not newlywocis, bathing in private. The very next month Hagi was off to the uncertainties of living en c! working in Belem, on the Amazon River, to clo electric fish experiments with colleagues from UCLA en c! abroad. He clic! not clo South America minimally but re- turnec! via Rio cle {aneiro, Buenos Aires, en c! Santiago, ap- parently enjoying the sights en c! adventures, meeting scien- tists, en c! collecting butterflies. In 1965 an invitation arrived from the Scripps Institution of Oceanography to be the first professor of neurobiology at the University of California at San Diego quite incle- penclently of the new meclical school, which was at the mo- ment creating the first Department of Neurosciences. Hagi was recruitec! by the marine biology division of Scripps. Some credit is certainly clue the late, great comparative physiologist, Prof. P. F. Scholancler, on the faculty of that division en c! to the then-clirector of the UCLA Brain Re- search Institute, John D. French, who had persuaded the Scripps faculty to cosponsor with the institute a unique, and for many years jointly operated, marine neurobiology facility on the third floor of Scholander's new Physiological Research Laboratory. A popular hypothesis is that the ma- rine biologists remembered the elegant electrophysiologi- cal demonstrations of functions of sense organs in fish by Yasuji Katsuki, Hagi's sponsor, en c! Yngve Zotterman from

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SUSUMU HAGIWARA 65 Stockholm, Hagi's first foreign host, cluring their short vis- its years before. In the transition period, prior to moving to La JolIa, Hagi spent a period between May and August of 1965 as a visiting professor at the College de France and publisher! several papers in French with Thomas Szabo. With a group of postdoctoral associates, Hagiwara initi- ated the Marine Neurobiology Facility of Scripps and the Brain Research Institute. He enjoyoc! four years of iclyIlic existence en c! outstanding scientific creativity in La {olIa. The maiden voyage of the unique research vessel Alpha He- li~c, createc! by Scholancler as an arm of the Physiological Research Laboratory en c! a national really international- facility for comparative biochemistry en c! physiology in re- mote habitats, set off for the Great Barrier Reef in the spring of 1966. Hagi en c! Kunitaro Takahashi en c! chief sci- entist Bullock were among the ten scientists in the first three-month program. Many vignettes of that great experi ence crows! into memory. One was clue to the chance that the three visitor! Bora Bora on the way to Australia en c! fount! that a fellow guest at the seaside hotel was the great astronomer Bart Bok, who took them to the ens! of the pier en c! gave a private lecture on the Milky Way en c! Southern Cross as an introduction to the South Pacific. As this expe- clition prover! en c! many others subsequently confirmed, Hagi well exemplified the kind of bench scientist who could make goof! use of a few weeks in a laboratory at an exotic loca- tion. Telling incidents sharer! by Hagi on the Alpha Helix Op- eration BilIabong are recountec! in a book by P. F. Scholancler, Enjoying a Life in Science (University of Alaska Press, 1990~. Susumu and "Pete" Scholander were kindred souls in their eagerness to explore the worIc! of species en c! in their skill in finding specially favorable material for the study of fun- damental problems, about half the time planned ahead of

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66 B I O G RA P H I C A L EMOIRS embarking on an expedition en c! half the time cliscoverec! among the species that hac! not been anticipated. His South American experience was enIargec! in 1967 with a several- month trip to Chile, together with Alan Grinnell en c! Jarec! Diamond, to study synaptic mechanisms in giant squids at Monte Mar, the marine station near Valparaiso. A major storm aborter! that project by driving the squic! to other waters (for several years), but with customary ease Hagi fount! an icleal preparation in the muscle fibers of Chilean giant barnacles. Two years later he was off to New Guinea on an Alpha Helix expedition lee! by George Bartholomew, studying bats en c! collecting butterflies en c! carvings, again with Grinnell. A highlight of this trip was a stopover enroute at MarIon Branclo's atoll off Tahiti. In 1973 Hagi was orga- nizer en c! chief scientist of his own Alpha Helix expedition to the Great Barrier Reef, where he again worker! with blue- spottec! sting rays, as he hac! clone in 1966 on the maiden expedition. In 1969 he was entices! back to UCLA, a great Toss to San Diego en c! gain for Los Angeles. He en c! his wife, Satoko, macle an attractive home in West Los Angeles, clecoratec! not only with his great butterfly collection, mounter! bircis, en c! New Guinea wool! carvings but also scores of hanging plants en c! tanks with varieties of koi en c! tropical fish. In a short time he was namer! the Eleanor I. Leslie Professor of Neuroscience en c! enjoyoc! twenty happy en c! productive years at the Brain Research Institute en c! its ferry Lewis Neuro- muscular Research Center before succumbing in 1989 to an illness that clemanclec! respiratory reserves he hac! lost nearly half a century before. Whereas Hagiwara was best known for his contributions to membrane and channel biophysics, he made a wide vari- ety of important contributions to systems physiology at the integrative level. His pioneering series of papers on the

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SUSUMU HAGIWARA 67 souncI-proclucing muscle of cicadas starter! a pregnant line of research on its dynamics en c! neural control in Englanc! en c! the Uniter! States, showing that classical muscle physi- ology illuminates only a fraction of the properties of muscle that evolution has spun off. One of these studies was his own, in 196S, on the neuromuscular specialization in the wingbeat of hummingbirds. His analysis of sensory nerve impulse interval fluctuations is a stanciarc! reference point for a consiclerable later literature. He macle major contri- butions to synaptic physiology en c! to the integrative mecha- nisms of the nine-cellec! cardiac ganglion of lobsters. He playact a central role in the initial discovery of electroreceptors in weakly electric fish en c! in the further discoveries of mul- tiple types of electroreceptors and nerve impulse codes. Beginning in 1964 his concentration on ionic mechanisms in active membranes en c! especially on calcium channels became markocI. After the great advance en c! wicle accep- tance of the Hocigkin-Huxley concept of the sodium en c! potassium ion basis of the nerve impulse in the squid giant axon membrane, Hagi asker! himself four questions: (~) How wiclely can one apply the original soclium-potassium channel concept to electrical excitation among a variety of tissues in different animals? (2) What other voltage-gatec! membrane channels exist besicles the original sodium en c! potassium channels? (3) What are the biological functions of those other channels? (4) How clic! the various ion chan- nels evolve phylogenetically en c! how clo they clevelop onto- genetically? These questions led him to study preparations such as muscle fibers in barnacles, mussels, and amphioxus, eggs of starfish, annelicis, en c! Drosophila, mucipuppy hair cells, crus- tacean photoreceptors, chromaffin cells in rats, lymphocytes and tumor cells in mice, seminiferous tubule cells, pituitary cells, left-handed snail cells, and human T cells. Only a

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68 B I O G RA P H I C A L EMOIRS vastly flexible expertise en c! a clisciplinec! theoretical minciset conic! so successfully carry out the basic experiments, avoic! clilettantism, en c! glean the harvest of general principles within natural diversity that Hagiwara clicI. He was a princi- pal player cluring the years when the concept of one chan- nel for each of two or three ions was graclually replacer! by the unclerstancling of a multitucle of distinct channels for each ion, differing in proportions en c! distribution among cell types. Hagiwara's name is particularly associates! with calcium channels in cell membranes. Whereas the action potential hac! been acloquately accounted! for as a sodium spike for more than a clecacle, in 1964 Hagi en c! his colleagues recog- nized the calcium spike in an unlikely preparation the normally nonspiking muscle fiber of a giant barnacle. For a time this spike was regarclec! as a curious anomaly resis- tant to removal of external sodium but converter! from nonspiking to a spiking cell by injecting sodium if its anion was a calcium bincler like sulfate. He recounts, with charac- teristically self-cleprecating humor, how, cluring this perioc! when "the calcium channel was only fount! in miserable animals like crustaceans en c! was thought to play no impor- tant function in the human brain . . . I sufferer! tremen- clously from a minority Esic] complex," until time went by en c! calcium channels were fount! in a variety of tissues, including mammalian brains, en c! it became clifficult to name an excitable tissue that floes not possess calcium channels. He proposer! the rule that soclium spikes are fount! where the function of the action potential is propagation of an impulse and calcium spikes are found where action poten- tials are couplet! with effecter functions such as contrac tion, secretion, transduction, transmission, and biolumines cence. BertiT Hille, ten years ago, summarized: "Hagi twas] a

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SUSUMU HAGIWARA SELECTED BIBLIOGRAPHY 1948 75 Sound-producing activities of cicada. I. Effects of light. Kagaku 18:464 (in Japanese). On the charping rhythm of the bird, Hororunis cantons. Kagaku 18:468-69 (in Japanese). 1949 Sound-producing activities of cicadas. II. Interaction. Kagaku 19:40 (in Japanese). On the fluctuation of the interval of rhythmic excitation. I. Analysis on the interval between impulse of a motor unit during human voluntary movement. Rep. Physiol. Sci. Inst. Tokyo Univ. 3:19-24. 1950 On the fluctuation of the interval of rhythmic excitation. II. Analy- sis on impulses from stretch receptor of a frog muscle. Rep. Physiol. Sci. Inst. Tokyo Univ. 4:28-35 (in Japanese, Ph.D. thesis). 1953 With T. Wakabayashi. Mechanical and electrical events in the main sound muscle of cicada. Jpn. J. Physiol. 3:249-53. Neuromuscular transmission in insects. Jpn. /. Physiol. 3:284-96. 1954 With A. Watanabe. Action potential of insect muscle examined with intracellular electrode. Jpn. /. Physiol. 4:65-78. With I. Tasaki and A. Watanabe. Action potentials recorded from inside a Mauthner cell of the cat-fish. Jpn. /. Physiol. 4:79-90. Analysis of interval fluctuation of the sensory nerve impulses. Jpn. J. Physiol. 4:234-40. With H. Uchiyama and A. Watanabe. The mechanism of sound pro- duction in certain cicada with special reference to the myogenic rhythm in insect muscle. Bull. Tokyo Med. Dent. Univ. 1:113-24. With M. J. Cohen and Y. Zotterman. The response spectrum of taste fibres in the cat: a single fibre analysis. Acta. Physiol. Scand. 33:316- 52.

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76 BIOGRAPHICAL MEMOIRS 1955 With A. Watanabe. The effect of tetraethylammonium chloride on the muscle membrane examined with an intracellular microelec- trode. 7. Physiol. 129:513-27. 1956 With A. Watanabe. Discharges in motoneurons of cicada. 7. Cell Comp. Physiol. 47:415-28. Neuromuscular mechanisms of sound production in the cicada. Physiol. Comp. Oecologia 4:142-53. 1957 With T. H. Bullock. Intracellular potentials in pacemaker and inte- grative neurons of the lobster cardiac ganglion. 7. Cell Comp. Physiol. 50:25-47. With T. H. Bullock. Intracellular recording from the giant synapse of the squid. 7. Gen. Physiol. 40:565-77. With I. Tasaki. Capacity of muscle fiber membrane. Am. /. Physiol. 188:423-29. With I. Tasaki. Demonstration of two stable potential states in the squid giant axons under tetraethylammonium chloride. 7. Gen. Physiol. 40:859-85. With S. Saito. Mechanism of action potential production in the nerve cell of a puffer. Proc. Jpn. A cad. 33:682-85. 1958 Synaptic potential in the motor giant axon of the crayfish. 7. Gen. Physiol. 41:1119-28. With Y. Oomura. The critical depolarization for the spike in the squid giant axon. Jpn. /. Physiol. 8 :234-45. With I. Tasaki. A study on the mechanism of impulse transmission across the giant synapse of the squid. 7. Physiol. 143:114-37. 1959 With S. Saito. Membrane potential change and membrane current in supramedullary nerve cell of puffer. 7. Neurophysiol. 22:204-21. With A. Watanabe and S. Saito. Potential changes in synctial neu- rons of lobster cardiac ganglion. J. Neurophysiol. 22:554-72.

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SUSUMU HAGIWARA 77 With S. Saito. Voltage-current relations in nerve cell membrane of On chidium verruculatum. 7. Physiol. 148: 161 -77. With C. Edwards. Potassium ions and the inhibitory process in the crayfish stretch receptor. 7. Gen. Physiol. 43:315-21. 1960 Current-voltage relations of nerve cell membrane. In Electrical Activ- ity of Single Cells, ed. Y. Katsuki, pp. 145-57. Tokyo: Igakushion. With K. Kusano and S. Saito. Membrane changes in crayfish stretch receptor neuron during synaptic inhibition and under action of gamma-aminobutyric acid. 7. Neurophysiol. 23:505-15. With K. Ogura. Analysis of song of cicadas. 7. Insect Physiol. 5:259-63. 1961 Nervous activities of the heart in crustacea. Ergeb. Biol. 24:287-311. With K. Kusano. On the integrative synaptic potentials of Onchidium nerve cell. kin. 7. Physiol. 11:96-101. With K. Kusano and S. Saito. Membrane changes on Onchidium nerve cell in potassium-rich media. 7. Physiol. 155:470-89. With K. Kusano. Synaptic inhibition in giant nerve cell of Onchidium verruculatum. 7. Neurophysiol. 24:167-75. 1962 With K. Kusano and K. Negishi. Physiological properties of electroreceptors of some gymnotids. 7. Neurophysiol. 25:430-49. With H. Morita. Electrotonic transmission between two nerve cells in leech ganglion. J. Neurophysiol. 25:721 -31. 1963 With H. Morita. Coding mechanisms of electroreceptor fibers in some electric fish. 7. Neurophysiol. 26:551-67. 1964 With K. Naka and S. Chichibu. Membrane properties of barnacle muscle fiber. Science 143:1446-48. With K. Naka. The initiation of spike potential in barnacle muscle fibers under low intracellular Ca++. J. Gen. Physiol. 48:141-62. With S. Chichibu and K. Naka. The effects of various ions on rest

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78 B I O G RA P H I C A L EMOIRS ing and spike potentials of barnacle muscle fibers. 7. Gen. Physiol. 48:163-79. With H. Morita and K. Naka. Transmission through distributed syn- apses between two giant axons of the sabellid worm. 7. Comp. Physiol. 13:453-60. With G. Edwards and S. Chichibu. Relation between membrane po- tential changes and tension in barnacle muscle fibers. 7. Gen. Physiol. 48:225-34. 1965 Relation of membrane properties of the giant muscle fiber of a barnacle to internal composition. 7. Gen. Physiol. 48:55-57. With S. Nakajima. Tetrodotoxin and manganese ions: effects on action potential of the frog heart. Science 149:1254-55. With T. Szabo and P. S. Enger. Physiological properties of electroreceptors in the electrical eel, Electrophorus electricus. 7. Neurophysiol. 28:775-83. With T. Szabo and P. S. Enger. Electroreceptor mechanisms in a high-frequency weakly electric fish, Sternarchus albifrons. 7. Neurophysiol. 28:784-99. With T. Szabo. Le fonctionnement de curtains electrorecepteurs. Physiol (Paris) 57 (5) :707-8. 1966 J Membrane properties of the barnacle muscle fiber. Ann. N.Y. A cad. Sci. 137:1015-24. With S. Nakajima. Effects of the intracellular Ca ion concentration upon the excitability of the muscle fiber membrane of a bar- nacle . 7. Gen. Physiol. 49: 807-18. With S. Nakajima. Differences in Na and Ca spikes as examined by application of tetrodotoxin, procaine, and manganese ions. J. Gen. Physiol. 49:793-806. With T. Szabo. Effects de dephasage au niveau d'organes sensoriels participants au d'electrolocation. J. Physiol. (Paris) 58~2~:267-68. With T. Szabo. Exploration intracellulaire de ltepithelium sensoriel de la vesicule de Savi chez Torpedo marmorata. 7. Physiol (Paris) 58 (5) :621-22.

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SUSUMU HAGIWARA 1967 79 With K. Takahashi. Surface density of calcium ions and calcium spikes in the barnacle fiber membrane. 7. Gen. Physiol. 50:583- 601. With K. Takahashi. Resting and spike potentials of skeletal muscle timbres of salt-water elasmobranch and teleost fish. 7. Physiol. 190:499- 518. With T. Szabo. A latency-change mechanism involved in sensory coding of electric fish (Mormyrids). Physiol. Behav. 2:331-35. 1968 With K. Takahashi and D. lunge. Excitation-contraction coupling in a barnacle muscle fiber as examined with voltage clamp tech- nique. 7. Gen. Physiol. 51:157-75. With I. Cooke, J. Diamond, A. Grinnell, and H. Sakata. Suppression of the action potential nerve by nitrobenzene derivatives. Proc. Nail. A cad. Sci. U.S.A. 60:470-77. With S. Chichibu and N. Simpson. Neuromuscular mechanisms of wing beat in hummingbirds. Z. Vgl. Physiol. 60:209-18. With R. Gruener, H. Hayashi, H. Sakata, and A. Grinnell. A. Effect of external and internal pH changes on K and C1 conductances in the muscle fiber membrane of a giant barnacle. 7. Gen. Physiol. 52:773-92. 1969 With H. Hayashi and K. Takahashi. Calcium and potassium currents of the membrane of a barnacle muscle fibre in relation to the Ca-spike. 7. Physiol. 205:115-29. With H. M. Brown, R. Meech, and H. Koike. Current-voltage regula- tions during illumination: photoreceptor membrane of a bar- nacle. Science 166:240-43. 1970 With H. M. Brown, H. Koike, and R. W. Meech. Membrane proper- ties of a barnacle photoreceptor examined by the voltage clamp technique. J. Physiol. (London) 208: 385-413.

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80 B I O G RA P H I C A L 1971 EMOIRS With H. M. Brown, H. Koike, and R. W. Meech. Electrical character- istics of a barnacle photoreceptor. Fed. Proc. 30:69-78. With K. Toyama and H. Hayashi. Mechanisms of anion and cation permeations in the resting membrane of a barnacle muscle fiber. 7. Gen. Physiol. 57:408-34. With H. Koike and H. M. Brown. Hyperpolarization of a barnacle photoreceptor membrane following illumination. 7. Gen. Physiol. 57:723-37. With M. Henkart and Y. Kidokoro. Action potentials and excitation contraction coupling of muscle cells in Amphioxus. 7. Physiol. 219:232-33. With Y. Kidokoro. Na and Ca components of action potential in Amphioxus muscle cells. 7. Physiol. 219:217-32. 1972 With A. D. Grinnell. Adaptations of the auditory nervous system for echolocation: studies of New Guinea bats. Z. Vgl. Physiol. 76:41- 81. With A. D. Grinnell. Studies of auditory neurophysiology in nonecholocating bats, and adaptation for echolocation in one genus, Rousettus. Z. Vgl. Physiol. 76:82-96. With D. C. Eaton, A. E. Stuart, and N. P. Rosenthal. Cation selectiv- ity of the resting membrane of squid axon. 7. Membr. Biol. 9:373- 84. 1973 Ca spike. In Advances in Biophysics, vol. 4, ed. M. Koitani, pp. 71-102. Tokyo: University of Tokyo Press. 1974 With K. Takahashi. Mechanism of anion permeation through the muscle fibre membrane of an elasmobranch fish, Tacniura lymma. J. Physiol. 238:109-27. With Y. Kidokoro and M. Henkart. Electrical properties of obliquely striated muscle fibre membrane of Anodonta glochidium. J. Comp. Physiol. 90:321-38. With J. Fukuda and D. C. Eaton. Membrane currents carried by Ca,

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SUSUMU HAGIWARA 81 Sr and Ba in barnacle muscle fiber during voltage clamp. 7. Gen. Physiol. 63:564-78. With K. Takahashi. The anomalous rectification and cation selectiv- ity of the membrane of a starfish egg cell. 7. Membr. Biol. 18:61- 80. 1975 Ca dependent action potential. In Membranes, A Series of Advances, vol. 3, ed. G. Eisenman, pp. 359-81. New York: Marcel Dekker. With S. Ozawa and O. Sand. Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. 7. Gen. Physiol. 65:617-44. With S. Ozawa, K. Nicolaysen, and A. E. Stuarat. Signal transmission from photoreceptors to ganglion cells in the visual system of the giant barnacle. Cold Spring Harbor Symposium, vol. XL, pp. 563- 70. With O. Sand and S. Ozawa. Electrical and mechanical stimulation of hair cells in the mudpuppy. J. Comp. Physiol. A102:13-26. 1976 With K. Ikeda and S. Ozawa. Synaptic transmission reversibly condi- tioned by a single-gene mutation in Drosophila melanogaster. Nature 259~5543~:489-91. With S. Miyazaki and N. P. Rosenthal. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. 7. Gen. Physiol. 67:621-38. With M. Henkart. Localization of calcium binding sites associated with the calcium spike in barnacle muscle. 7. Membr. Biol. 27:1-20. With A. Miyazaki. Electrical properties of the Drosophila egg mem- brane. J. Dev. Biol. 53:91-100. 1977 With S. Miyazaki. Ca and Na spike in egg cell membrane. Prog. Clin. Biol. Res. 15: 147-58. With B. L. Brandt, Y. Kidokoro, and S. Miyazaki. Action potentials in the rat chromaffin cell and effects of acetylcholine. 7. Physiol. 263:417-39. With S. Miyazaki. Changes in excitability of the cell membrane dur

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82 B I O G RA P H I C A L EMOIRS ing "differentiation without cleavage" in the egg of the annelid, Chaetopterus pergamontaccus. 7. Physiol. 272:197-216. With S. Ozawa and K. Nicolaysen. Neural organization of shadow reflex in a giant barnacle, Blanus nubilus. 7. Neurophysiol. 40:982- 95. With S. Miyazaki, S. Krasne, and S. Ciani. Anomalous permeabilities of the egg cell membrane of a starfish in K+-T1+ mixtures. 7. Gen. Physiol. 70:269-81. 1978 Differentiation of Na and Ca channels during the early develop- ment. In Membrane Transduction Mechanisms, vol. 33, ed. R. A. Cone and J. E. Dowling, pp. 189-97. New York: Raven Press. With S. Miyazaki, W. Moody, and T. Patlak. Blocking effects of Ba and H ions on the K current during anomalous rectification in the starfish egg. J. Physiol. 279:167-85. With L. A. Taffe and R. T. Kado. The time course of cortical vesicle fusion in sea urchin eggs observed as membrane capacitance changes. 7. Dev. Biol. 67:243-48. With S. Ciani, S. Krasne, and S. Miyazaki. A model for anomalous rectification: electrochemical-potential-dependent gating of mem- brane channels. 7. Membr. Biol. 44:103-34. 1979 With L. A. Taffe. Electrical properties of egg cell membranes. Annul Rev. Biophys. Bioeng. 8:385-416. With Y. Kidokoro and A. Ritchie. Effect of tetrodotoxin on adrena- line secretion in the perfused rat adrenal medulla. Nature 278:63- 65. With M. Yoshii. Effects of internal K and Na on the anomalous rectification of the starfish egg as examined by internal perfu- sion. J. Physiol. 292:251-65. 1980 The Ca ion permeability of the cell membrane. Jpn. Circ. J. 44:239- 48. With S. Ciani and S. Krasne. A model for the effects of potential and external K+ concentration of the Cs+ blocking of inward rec- tification. Biophys. J. 30: 199-204.

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SUSUMU HAGIWARA 83 With M. Yoshii. Effect of temperature on the anomalous rectifica- tion of the membrane of the egg of the starfish, Mediaster acqualis. 7. Physiol. 307:517-27. 1981 Membrane potential dependent Ca channels. In Physiology of Excit- able Membrane, ed. T. Salanki, pp. 105-8. General considerations in the study of the Ca++ channel. In Mollus- can Nerve Cell: Biophysics to Behavior, vol. 1, ed. T. Koester and H. Byrne, pp. 33-40. Cold Spring Harbor Report in Neurosciences. General properties of gated Ca transport. In Mechanism of Gated Calcium Transport Across Biological Membranes, ed. S. T. Ohnishi and M. Endo, pp. 3-9. New York: Academic Press. With L. Byerly. Membrane biophysics of calcium currents. Fed. Proc. 40:2220-25. With L. Byerly. Ca channel. Annul Rev. Neurosci. 4:69-125. With S. Yoshida and M. Yoshii. Transient and delayed K currents in the egg cell membrane co-elenterate, Renilla koellikeri. 7. Physiol. 318:123-41. With H. Ohmori and S. Yoshida. Single K+ channel currents of anomalous rectification in cultured rat myotubes. Proc. Natl. Acad. Sci. U.S.A. 78:4960-64. 1982 With L. Byerly. Calcium currents in internally-perfused nerve cell bodies of Limnea stagnalis. J. Physiol. 322:503-28. With W. T. Moody. Block of inward rectification by intracellular H+ in immature starfish oocytes of the starfish Mediaster acqualis. 7. Gen. Physiol. 79:115-30. With H. Ohmori. Studies of calcium channels in the rat clonal pitu- itary cells with patch electrode voltage clamp. J. Physiol. 331:231- 52. 1983 Ion Channels in Cell Membrane: Phylogenetic and Development Approaches. Distinguished Lecture Series of General Physiologists Society. New York: Raven Press. With L. Byerly. Ca channel. Trends Neurosci. 6:189-93.

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84 B I O G RA P H I C A L EMOIRS With H. Ohmori. Studies of single calcium channel currents in rat clonal pituitary cells. 7. Physiol. 336:649-61. With Y. Fukushima. Voltage-gated Ca channel in mouse myeloma cells. Proc. Natl. Acad. Sci. U.S.A. 80:2240-42. 1984 With Y. Fukushima and M. Henkart. Potassium current in clonal cytotoxic T lymphocytes from the mouse. 7. Physiol. 351:645-56. With K. Kawa. Calcium and potassium currents in spermatogenic cells dissociated from rat seminiferous tubules. 7. Physiol. 356:135- 49. With Y. Fukushima and R. E. Saxon. Variations of calcium current during the cell growth cycle in mouse hybridoma lines secreting immunoglobulins. 7. Physiol. 355:313-21. 1985 With Y. Fukushima. Currents carried by monovalent cations through calcium channels in mouse neoplastic B lymphocytes. 7. Physiol. 358:225-84. 1986 With Y. Fukushima. Ion channels of lymphocytes. In Comparative Neurobiology: Modes of Communication in Nervous Systems, ed. F. Strumwasser and M. Cohen, pp. 119-31. New York: Wiley and Sons. With L. Schlichter and N. Sidell. Potassium channels mediate kill- ing by human natural killer cell. Proc. Natl. A cad. Sci. U.S.A. 83:451- 55. With T. Iijima and S. Ciani. Effects of the external pH on Ca chan- nels. Experimental studies and theoretical considerations using a two-site, two-ion model. Proc. Natl. Acad. Sci. U.S.A. 83:654-58. With L. Schlichter and N. Sidell. K channels are expressed early in human T cell development Proc. Natl. A cad. Sci. U.S.A. 83:5625- 29. With N. Sidell, L. C. Schlichter, S. Wright, and S. H. Golub. Potas- sium channels in human NK cells are involved in discrete stages of the killing process. J. Immunol. 137:1650-58.

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SUSUMU HAGIWARA 1987 85 With T. Iijima. Voltage dependent K channels in protoplasts of trap-lobe cells in Dionae muscipula. I. Memb. Biol. 100:73-81. 1988 With L. Byerly. Calcium channel diversity. In Ion Channel Modula- tion, ed. A. D. Grinnell, D. L. Armstrong, and M. B. Jackson, pp. 3-18. New York: Plenum Press. With T. Hirano. Synaptic transmission between rat cerebellar gran- ule and Purkinje cells in dissociated cell culture: effects of excitatory- amino acid transmitter antagonists. Proc. Natl. A cad. Sci. U.S.A. 85:934-38. With E. E. Serrano and E. Zeiger. Red light stimulated an electro- genic proton pump in Vicia guard cell protoplast. Proc. Natl. A cad. Sci. U.S.A. 85:436-40. 1989 With T. Hirano. Kinetics and distribution of voltage-gated Ca, Na and K channels on the somata of rat cerebellar Purkinje cells. Flugers Archiv. Eur. I. Physiol. 413:463-69. 1990 With V. Corvalan, R. Cole, and J. de Vellis. Neuronal modulation of calcium channel activity in cultured rat astrocytes. Pro c. Natl. Acad. Sci. U.S.A. 87:4345-48. With J. I. Schroeder. Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of non-selective Ca2+ permeable channels. Proc. Natl. Acad. Sci. U.S.A. 87:9305-9. With N. Yamashita. Membrane depolarization and intracellular Ca2+ increase caused by high external Ca2+ in a rat calcitonin-secret- ing cell line. 7. Physiol. 431:243-67. With N. Yamashita and S. Ciani. Effects of internal Na+ on the Ca channel outward current in mouse neoplastic B lymphocytes. 7. Gen. Physiol. 96:559-79.