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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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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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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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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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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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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
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Representative terms from entire chapter:
barnacle muscle
