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Eccles was born in Melbourne, Australia. He grew up there with his two sisters and his parents: William and Mary Carew Eccles (both teachers, who home schooled him until he was 12). He initially attended Warrnambool High School (now Warrnambool College) (where a science wing is named in his honour), then completed his final year of schooling at Melbourne High School. Aged 17, he was awarded a senior scholarship to study medicine at the University of Melbourne. As a medical undergraduate, he was never able to find a satisfactory explanation for the interaction of mind and body; he started to think about becoming a neuroscientist. He graduated (with first class honours) in 1925, and was awarded a Rhodes Scholarship to study under Charles Scott Sherrington at Magdalen College, Oxford University, where he received his Doctor of Philosophy in 1929.

In 1937 Eccles returned to Australia, where he worked on military research during World War II. After the war, he became a professor at the University of Otago in New Zealand. From 1952 to 1962 he worked as a professor at the John Curtin School of Medical Research (JCSMR) of the Australian National University. The Eccles Institute of Neuroscience will be headquartered in a new $60 million wing of JCSMR from 2012.