It's the first time an uncommunicative, severely brain-injured patient has been able to give answers clinically relevant to their care.
Scott Routley, 39, was asked questions while having his brain activity scanned in an fMRI machine.
His doctor says the discovery means medical textbooks will need rewriting.
Vegetative patients emerge from a coma into a condition where they have periods awake, with their eyes open, but have no perception of themselves or the outside world.
Mr Routley suffered a severe brain injury in a car accident 12 years ago.
None of his physical assessments since then have shown any sign of awareness, or ability to communicate.
But the British neuroscientist Prof Adrian Owen - who led the team at the Brain and Mind Institute, University of Western Ontario - said Mr Routley was clearly not vegetative.
"Scott has been able to show he has a conscious, thinking mind. We have scanned him several times and his pattern of brain activity shows he is clearly choosing to answer our questions. We believe he knows who and where he is."
Prof Owen said it was a groundbreaking moment.
"Asking a patient something important to them has been our aim for many years. In future we could ask what we could do to improve their quality of life. It could be simple things like the entertainment we provide or the times of day they are washed and fed."
Scott Routley's parents say they always thought he was conscious and could communicate by lifting a thumb or moving his eyes. But this has never been accepted by medical staff.
Prof Bryan Young at University Hospital, London - Mr Routley's neurologist for a decade - said the scan results overturned all the behavioural assessments that had been made over the years.
"I was impressed and amazed that he was able to show these cognitive responses. He had the clinical picture of a typical vegetative patient and showed no spontaneous movements that looked meaningful."
Observational assessments of Mr Routley since he responded in the scanner have continued to suggest he is vegetative. Prof Young said medical textbooks would need to be updated to include Prof Owen's techniques.
The BBC's Panorama programme followed several vegetative and minimally-conscious patients in Britain and Canada for more than a year.
Another Canadian patient, Steven Graham, was able to demonstrate that he had laid down new memories since his brain injury. Mr Graham answers yes when asked whether his sister has a daughter. His niece was born after his car accident five years ago.
The Panorama team also followed three patients at the Royal Hospital for Neuro-disability (RHN) in Putney, which specialises in the rehabilitation of brain-injured patients.
It collaborates with a team of Cambridge University neuroscientists at the Wolfson Brain Imaging Centre at Addenbrooke's hospital, Cambridge.
A second patient, who was not able to be fully assessed by the RHN because of repeated sickness, is later shown to have some limited awareness in brain scans.