Basically you have to decide what is most important to you. Do you want to have the widest range of content offerings(Roku), or the best compatibility between other Apple devices and software(Apple TV)?
The Roku box for example can play Hulu and Hulu Plus. The Hulu service is in very high demand and a very good content stream for the Roku. The Apple TV at this time will not play it out of the box, although it can be hacked to do so.
The biggest advantage that the Apple TV has is if you own or plan to use an iOS device in conjunction with it. For example, you can use AirPlay to stream music, photos, video, and apps to your Apple TV. This can be very handy in many situations. If you don't already have an iPhone, iPad, or the like - and don't plan on getting one anytime soon, then this shouldn't be a big draw.
The Apple TV also works flawlessly with iTunes. For example you can use iTunes Match then stream the audio to your Apple TV very easily. Roku can do some similar things with iTunes, but is does not have the same level of integration.
Overall, both devices have benefits and downsides, it just depends what you think your primary use will be and what hardware ecosystem you have. For more detailed information I would take a look at this review that compares the two.
The only super major differences the 1st Gen Apple TV's has from the new ones is the ability to store Movies, Music, Content, etc because they have a physical hard drive in them for doing those things. The other things is that they can connect to TV's through Red, Blue, Green Component Cables. They also do not support Airplay with out a hack or a software fix. Also, the newest Apple TV, the 3rd Gen, allows for 1080p HD playback, where the older ones only support 720p HD playback.
There are also a few other minor differences in size, power consumption, software options/OS and so on.
The new Apple TV's do not have hard drives or Component Cable outputs and support Airplay out of the box. Airplay is probably the biggest feature that makes people who don't want to hack to jump ship to the newer box. It is pretty cool. The 1080 HD playback is nice, but depending on your TV, may or may not be noticeable/important.
Some people like the older ones also because they can be hacked and used as linux computers (link) with actual storage and since they can also store things on them, you can take it with you and have videos/music on it and not require internet for streaming your content.
Though the biggest reason is most likely the hack-ability of them, they are tiny computers with a decent amount of power. And since they aren't sold any more and are still sought after, that would explain their above average price.
The new Apple TV's require internet of some kind or at least a local network for stream video and movies and data from a computer or the internet.
They are also significantly smaller too, the older Apple TVs are much larger.
You can see all the differences on their wiki page, it lays out the differences in features between the devices and even talks about most of the hacks that are available. Very informative.
I hope that this answer helps you out.
Apparently not much these days unless you want to play standard definition content or heavily mod the thing.
See here for more info on making it into a useful device for that purpose (Kodi can be configured to stream media from those services you mentioned):