Earlier in the month, Thompson claimed that the BBC's newsrooms had a "massive bias to the left" when he joined the corporation in 1979.
Veteran broadcaster Bolton, who was Thompson's manager when he edited Nationwide, said that he was left "baffled and rather irritated" by the director general's comments, reports The Guardian.
Writing in a letter published in the BBC's in-house magazine Ariel, Bolton said: "Perhaps he believes my fellow programme editors of that time like Chris Capron, George Carey, Ron Neil, Peter Ibbotson and Hugh Williams were lefties?
"In which case he must be possessed of remarkable insight since even today I don't know what their political leanings were or are. How about the main presenters then, Robin Day, David Dimbleby, John Tusa, Peter Snow, Frank Bough, Sue Lawley. Card-carrying Commies? I don't think so.
"What about the rows with the Thatcher government? Ah the rows! Well I was involved in quite a few of them and they weren't about whether we were pro or anti Mrs Thatcher; they were about whether we should report as honestly and openly as we could about the situation in Northern Ireland or the Falklands War."
Bolton added: "Of course everyone has views. It is undeniable that most editorial staff were, and probably are, of a liberal inclination when it comes to social issues, and that they cluster around the middle ground of the political spectrum.
"I would also suggest they are predominantly secular as well. We all have biases, the crucial thing is to be aware of them. However it is something else entirely to suggest that we flawed creatures made predominantly left-wing programmes. When he worked for me, Mark used to do his research. In this case he clearly has not."