Neuroimaging (for example, functional magnetic resonance imaging) signals are taken as a uniform proxy for local neural activity. By simultaneously recording electrode and neuroimaging (intrinsic optical imaging) signals in alert, task-engaged macaque visual cortex, we recently observed a large anticipatory trial-related neuroimaging signal that was poorly related to local spiking or field potentials. We used these same techniques to study the interactions of this trial-related signal with stimulus-evoked responses over the full range of stimulus intensities, including total darkness. We found that the two signals could be separated, and added linearly over this full range. The stimulus-evoked component was related linearly to local spiking and, consequently, could be used to obtain precise and reliable estimates of local neural activity. The trial-related signal likely has a distinct neural mechanism, however, and failure to account for it properly could lead to substantial errors when estimating local neural spiking from the neuroimaging signal.