If you try to hold down one of the horizontal arrow keys or the backspace, it only happens once and won't happen again, it seems like it only happens with client-side screens, but i didn't check it here. Also LibGUI is affected by the very same bug, so it might be a vanilla-related problem?

Yes you can, but it breaks seemingly randomly. Up to this day I have no idea why. It does seem to be a vanilla issue though.