Here's page 15 from the owner's manual for a 1977 Honda CB400F. You decide what it means.
On my 1976 400F, the front running lights (the 1157's in the front signal light housings) are on only with the low beam. Selecting high beam turns those running lights off (but of course does not effect the signalling capability of those lamps). And mb is right - the stock winker uses only two (of the three) connections.
When I bought my bike, coincidentally I had the same signal light issues as you have now. I replaced the winker with a NOS OEM winker. I also learned to keep the battery charged. I found that my battery could still run the bike, but below a certain charge level, I found that the signal light function became erratic at best. More often they just stayed on when I slid the signal switch.
Since I was a rank beginner at the time, it took me a week or two to learn how to keep the rpms up sufficiently enough to keep the battery happy. I also made (and still make) it a habit to start the bike with the kick starter whenever possible. That kept the winker happy too, for my first season of riding.
Last winter I replaced the wiring harness, installed an electronic voltage regulator, replaced the left hand handlebar switch with a new one, stuck a voltmeter on the gauge cluster, and wired in an (illegal) headlight switch. Even after all that, occasionally my signals still freeze on, but that's only when the battery is down somewhat. After a few blocks they always get back to working decently again.
When I wired in the new handlebar switch I could never get those run lights to work again. I have a few ideas why that is, and I plan to repair them over the next few weeks.
My other electrical task for the next month or so is to swap out my bulbs to LED bulbs (including changing over to an electronic winker). I've calculated that I could save enough juice doing that, so that I will be able to operate some sort of hand-warming system on my little bike.
I would like warmer hands .....
But if I can't do that somehow, I'll use the extra power to upgrade the headlight to something with a little more punch.