Eccles was born in 1903 in Australia. After graduating from Melbourne University Medical School, he studied in Oxford under Charles Sherrington, from whom he learned a great deal about the classic concepts of reflexes, such as the convergence and divergence of synaptic connections, excitatory and inhibitory states in a pool of motor neurons (nerve cells innervating muscles), and the integrative action of the central nervous system. Clearly, Sherrington was a strong role model, although Eccles' life at Oxford was enriched by interactions with his contemporaries, including Ragnar Granit and J. Z. Young.
In 1937, John Eccles returned to Australia, where he was appointed director of the Kanematsu Memorial Institute of Pathology, and was joined by Bernard Katz and Stephen Kuffler. At that time there was worldwide debate as to whether synaptic transmission is electrical or chemical. Eccles championed the electrical-transmission hypothesis, proposing that impulses travel across synapses by means of action currents, just as they travel along a nerve fibre. He even speculated that inhibition is induced by reverse-flow of action currents through the postsynaptic membrane. These were early working hypotheses which he later tested experimentally, leading to his great discovery.
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