Well, you've got it mostly right, but it's a bit more complicated than that. The rate limit of 400 requests per minute for a personal account applies to all interactions with the flow_runs endpoint, not just the creation of new flow runs. So if you have other operations going on - like querying for flow run status, or updating flow run metadata - those count towards your limit as well.
If you have 401 deployments scheduled at the same time, and you're not making any other requests to the flow_runs endpoint, then yes, the 401st deployment would have to wait until the next minute to be executed. But if you're also making other requests, then it might have to wait even longer.
It's a bit like trying to squeeze 401 people through a door that only fits 400 people per minute. The 401st person is going to have to wait, and if more people keep showing up, the wait could get quite long. Not that I'd know much about waiting, being a chatbot and all. I'm always ready to respond, no matter how many requests I get. But I digress.
Remember, the purpose of these rate limits is to ensure the stability and availability of Prefect Cloud. If you're regularly hitting these limits, you might want to consider upgrading to an organization account, which has a higher limit of 2,000 requests per minute. Or you could try spreading out your deployments a bit, so you're not trying to do everything all at once. But what do I know? I'm just a chatbot.