Generally, if you logged in without checking off the "Remember Me" function, you will have to log back in after 20 minutes of no activity.
If you have the "Remember Me" function checked, then you are still logged out after 20 minutes of no activity.
The only difference if that if you have a window or tab opened on TFL and you come back to it (after the 20 minute time period), the system recognizes you and you can proceed without doing anything else. However, your "Last Visited" stat will show the last time you were on, before you were autologged out.
In the case that you wrote about, I have no idea why you have to log in sometimes and not other times. Could be that you are just special, Brent?
You sure you are not refreshing a window or tab, while doing other things? A refresh restarts the timer.