I've noticed this over the last couple versions. I've only used WordPress this year so I can't really speak for anything earlier than version 2.5. (I also apologize if this is covered elsewhere. I tried several searches and didn't see anything relevant.)
I don't think the counter showing how many plugins have updates works correctly. Yesterday the counter showed 3 plugins. As I went plugin by plugin I wound up updating 5! It always seems that WordPress finds more updates once I've updated the first one. Yet the Extend page for the plugin says it was last updated several hours ago.