For a lot of applications (ie browsing), I wonder if setting the hard drives on a very short power cycle (turn off after 3 minutes of non-use maybe?), combined with several sticks of 256MB RAM would help keep the drives from spinning?

Only with certain programs now. Unless your browser allows for a no disk cache option, browsing would spin the drive back up every change of the page. And most applications now auto save your work in case a crash occurs. I have to admit that browsing on a completly silent machine is awesome, but rare. I used to queue up several pages on my Solo laptop, let the drive spin down, and read web pages in the silence of my room at night.