In Lion, the "Open File" dialog doesn't refresh until 30 to 60 seconds after the window appears
I don't know if this is relevant, but many times when I go to any kind of file dialogue or even just click on some tool or something, I get a few seconds (or more) of beach ball while my second HD (non-boot drive with most of my documents/non-OS files) wakes up and gets up to speed. I can hear it revving up and when it gets to speed the OS unfreezes… so maybe if your file directories are being cached in memory or the drive cache, when the HD wakes after 30 secs for whatever reason, it updates the directory lists in memory?

I'm thinking this isn't super common complaint so maybe it's HD settings specific like my problem (I think I set my 2nd HD to have energy saving options somewhere when I installed it and haven't found a way to have it spinning 24x7.