Quick workaround: Before typing in an emacs window that displays this behavior, move the mouse cursor to a region of the window where Ctrl-mouse-1 has no effect (eg. the top "window handle" region. Now you can type without fear of having the buffer menu popup on you every so often. (I hope).
The permanent fix is somewhere outside of emacs, either in the window manager, or X11 configuration. By default, emacs has variable: make-pointer-invisible set to t (true) which will cause proper behavior when typing. Something external to emacs is causing emacs to only sometimes hide the pointer when typing.
Hope this helps.