You're right, if they were showed up earlier then they should show up now.
One thing you might try is to copy tpl_modules_additional_images.php to
includes/templates/comstock/templates
see if that makes a difference.
I don't even know what "zen lightbox" is...
I don't know if this will help.. but when I switch to apple_zen (which did not have jscrip_imagehover.js in the template) I did not have this behavior; when I put in the jscript - same problem.
However, this works fine in classic (with the jscript_imagehover.js in)
I tried to remove this jscript from comstat template, but it made no difference.
Basic but vital question -
do you have all of your additional images uploaded to your images directory?
Also, on the question of the "top of the page behavior"
in your includes/templates/template_default
make a copy the folder popup_image_additional and place it in
includes/templates/comstock
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