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I had a general question regarding the Intel(R) 82801FB/FBM USB Universal Host Controller (ICH6). The ICH6 has five USB Host controllers in it, with (I'm assuming) two physical USB ports per controller.

My Question is, does the ICH6 or any Intel SouthBridge supply up to 500mA per physical USB port, or does it share the 500mA per Host controller between the two USB ports on each controller?

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If you read the document that you linked in, you'll find that the ICH6 itself does not supply the current for the USB port at all, as there's no pin for that on the chip. Instead, an external circuit is used for that. This is a pretty standard way to implement power to USB host ports.

There are several ways to implement the USB power supply, the simplest way is to connect it directly or through a PTC to +5V, like in Raspberry Pi:

enter image description here

This way you may draw from the USB port as much as the power supply (or the PTC) allows, and a short circuit will likely disrupt the operation of the host.

Or a special USB load switch IC may be used, which can limit the current to some fixed or configurable value and/or may be used to completely switch off the power to that port, like the SY6280 in Marsboard:

enter image description here

There are also USB load switch ICs that are able to indicate overcurrent situation back to the host, like the LM3526 in an LPC17xx board:

enter image description here

So, how much current you may draw from your USB ports without getting into trouble, and what happens if you draw too much, totally depends on the circuit used to power your ports (and sometimes the software configuration as well), outside your SouthBridge. You may examine your board and try to trace the USB power lines to see what ICs are there (they are usually very close to connectors), and then reading the data sheets might give you some clue.

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