Yeah, the folders should be the same, just stored on the same device the games come from (and in the case of the internal HDD, on the +OPL partition as you discovered). Just make sure that all the discarts and boxarts are in a folder called ART inside of the +OPL partition. Other folders are CFG for per-game configurations, THM for OPL themes, and VMC for virtual memcards. Contents of all of these folders can be copied between devices and will function properly.
Chip-free/MC-free homebrew <3
FMCB 1.93 on MC for emergencies, NA
250GB HDD/FHDB 1.93/OPL 0.9.2 (GSM and non-GSM)/PS2 games, NO HDDOSD
80GB HDD/FHDB 1.93/POPStarter rev12/OPL644/GSM0.37/PS1 games, NO HDDOSD
SCPH-75001 (sitting idle, slims suck):
FMCB 1.92 on MC