I signed up for this forum just to answer your question!
I've been having the exact same problem in After Effects and I've been pulling my hair out trying to backtrack my steps over the past couple of months to try and figure out what had changed in my laptop's configuration. You're never going to believe what was causing it (at least for me)
Microsoft IntelliPoint Drivers (v6.1) was the culprit!
I tried tweaking the settings within the Intellipoint control panel, but in the end, the only thing that worked was uninstalling Intellipoint altogether. Now my After Effects is annoyance free! And to think that it only took me 6 hours to troubleshoot that...
Why did I think that it might have been the IntelliPoint? Well, I decided to see if I would get the same jittery windows in AE if I navigated the menus with the keyboard, and didn't... so I figured that it was some sort of mouse focus related thing and remember the recent acquisition of one Microsoft Wireless Notebook Mouse.
Ugh. I can't even begin to speculate on what Microsoft added to the driver that would turn the normally benign mouse pointer evil.
Please let me know if this info was related to the problems you were having.