WordPress "unaware" of updates - how to fix?

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I have two WordPress installs on InMotion. I've discovered that one site is somehow "not aware" of updates.

One the site that works (let's call this "Working Site"), this is what it looks like when I login and updates are available:
http://postimg.org/image/3obftgrk1/
Note that Updates in the sidebar shows a red circle with the number of updates (these are plugin updates by the way).

On the second site (let's call this "Malfunctioning Site"), when I log in and updates are available, Updates in the sidebar is NOT showing a red circle with the number of updates. This is what it looks like:
http://postimg.org/image/tyshe5zqn/
N.B. When I took this screenshot, the plugins that had updates were the same between the two sites (except for one).

On the Malfunctioning Site, if I manually click Updates in the sidebar, then it seems to "recognize" that, and then Updates in the sidebar does show a red circle. This is what it looks like subsequently (which looks like Working Site):
http://postimg.org/image/qxk99grk1/

Both installs were made identically (using Softaculous, and have NOT selected "Disable Update Notifications"), and I have set them up in an identical fashion on the backend, including their wp-config.php files. Most of the plugins are the same too. In addition, I have another site on another web host set up also in an almost identical fashion, and that site behaves just like the Working Site.

The only main differences between the Malfunctioning Site and the Working Site are that one uses HTTPS and the other does not, and they use different themes. However, the site I mentioned on the other web site is using a different theme as well, and it works like the Working Site.

One more discrepancy is that Working Site automatically updated to WordPress 4.4.2, whereas Malfunctioning Site did not, and also didn't show Update in the sidebar with a red circle, although it did note it at the top of the Dashboard. Screenshot of Malfunctioning Site today:
http://postimg.org/image/vd93xpp43/

This problem is not super grave, but the aspect that is annoying is that the inability of Malfunctioning Site to be fully "aware" of updates means that plugins that have a behaviour when there are updates do not function properly. For example, I have WordFence installed on all three sites in identical fashion, and while it sends emails when updates are available to the Working Site (and my site on the other web host), it doesn't send such emails for Malfunctioning Site since WordPress is not fully detecting the updates being available.

Has anyone ever experienced such an issue? I tried to contact InMotion Support via email and chat, and they suggested I make a post about it. I appreciate all help!!
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IMH Support Agent 5
Yes, I also am not sure what could cause a disruption in the system updates. It is possible themes and plugins play a role in the back end because they can control PHP functions in a variety of different ways not always visible, but you certainly do not have to troubleshoot them if you don't want to. However, it would be good to check those off the list of possible causes.
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IMH Support Agent 5
Hello antoinmo, Thank you for contacting us about your WordPress error. There a re a definitely a few things you can try right away. I advise checking out our WordPress Troubleshooting Guide and enable debug mode. Then you can load the site with the default theme. If that does not help then you can try loading the site with plugins deactivated. Thanks for your question. Let us know if you have any further difficulty. Best, Christopher M.