Screen Blackouts When Browsing Computer

I recently cleaned my computer (got dust out and repasted the heat sink on my processor). I wouldn't even consider myself an amateur computer person, but I know how to use Google and can generally troubleshoot common problems.
 
To the point: At some point after I put my computer back together and hooked it up to my monitor (that had no previous problems) it started going black for 1 - 2 seconds while I use File Explorer (just browsing) on my computer. The problem is frequent but inconsistent as to when it will do it. If I'm doing something and need to navigate, after opening a file it will sometimes just go black for 1 - 2 seconds and come back as if nothing happened. If say I acted as though the monitor did not go black and pressed enter on a highlighted file, when the monitor refreshed properly whatever I did executed properly.If I'm watching a movie or playing a video game or browsing the internet* or alt-tab between programs on already opened files I do not have this problem. It only occurs when I browse files on my harddrive.
 
*after I wrote this I went to watch an embedded youtube video and pressed play and it did blink for less than a second after I hit the play button (did not go full screen yet). If I notice anything else I will update this.
 
One very peculiar thing and I don't even know if it's related or not, is if I leave my computer idle for 2 - 3 hours and come back I cannot get the screen to come up at all (the monitor acts like there is no input) and not only that, my computer reset button is unresponsive. I literally have to do a hard reboot to get my computer to respond. This only happens if I leave it alone for long periods. It doesn't happen as long as I'm using the computer.