British and Belgian researchers used a brain scanner called functional magnetic resonance imaging to show the man, who suffered a severe traumatic brain injury in a road accident in 2003, was able to think yes or no answers to questions by wilfully changing his brain activity.
Experts say the result means all patients in coma-like states should be reassessed and it may change the way they are cared for in future.
After detecting signs of awareness, the doctors scanned the man's brain while he was asked to say yes or no to questions such as is your father's name Thomas?. The results showed that by changing his brain activity, the man communicated his answer.
We were astonished when we saw the results of the patient's scan and that he was able to correctly answer the questions that were asked by simply changing his thoughts, said Adrian Owen, co-author of the study from the Medical Research Council.
Not only did these scans tell us that the patient was not in a vegetative state but, more importantly, for the first time in five years it provided the patient with a way of communicating his thoughts to the outside world.
The man, now 29 years old, was one of 23 patients diagnosed as being in a vegetative state who were scanned using functional magnetic resonance imaging (fMRI).
The scans detected signs of awareness in four of the patients, the researchers wrote in their study published in the New England Journal of Medicine on Wednesday.
The fMRI method used can decipher the brain's answers to questions in healthy people with 100 percent accuracy, but it has never been tried before in patients unable to move or speak.
Nicholas Schiff, a neurologist from Weill Cornell Medical College in New York, said the findings were a game changer that could have a profound impact across medicine.
In comments sent by email, he said the results called for the reassessment of all patients currently in so-called minimally conscious or vegetative states.
Allan Ropper of Brigham and Women's Hospital in Boston said the study suggested such scans may be one more test doctors can use on people who recover from a coma but remain unresponsive.
In an online commentary on the study, Ropper stressed that brain activation was detected in very few patients and only those with a traumatic injury, not in cases where the whole brain had been damaged by oxygen starvation.
A bitter right-to-die row erupted in the United States in 2005 over the fate of Terri Schiavo, a 41-year-old woman who had been in a vegetative state since a heart attack in 1990.
Schiavo's case went back and forth through the U.S. courts and even prompted then President George W. Bush to intervene as her husband fought for doctors to halt feeding and let her die.
Experts say traumatic brain injury can heal better than injury from stroke or heart attack, such as Schiavo suffered.
A similar case in Italy involved a comatose woman whose father had battled for 10 years to have her feeding tube disconnected. Eluana Englaro died last year.
(Additional reporting by Gene Emery; Editing by Charles Dick)