Neuronal population activity in macaque visual cortices dynamically changes through repeated fixations in active free viewing.

During free viewing, we move our eyes and fixate on objects to recognize the visual scene of our surroundings. To investigate the neural representation of objects in this process, we studied individual and population neuronal activity in three different visual regions of the brains of macaque monkeys ( Macaca fuscata ): the primary and secondary visual cortices and the inferotemporal cortex. We designed a task where the animal freely selected objects in a stimulus image to fixate on while we examined the relationship between spiking activity, the order of fixations, and the fixated objects. We found that activity changed across repeated fixations on the same object in all three recorded areas, with observed reductions in firing rates. Furthermore, the responses of individual neurons became sparser and more selective with individual objects. The population activity for individual objects also became distinct. These results suggest that visual neurons respond dynamically to repeated input stimuli through a smaller number of spikes, thereby allowing for discrimination between individual objects with smaller energy. Significance Statement Conventionally, ventral visual neurons, which are crucial for object recognition, have been studied under passive viewing conditions that involve forced fixation in fixation tasks. However, the importance of investigating visual perception under active conditions is gaining recognition. We studied individual and population neuronal activity in three different ventral visual areas of the brains of macaque monkeys-V1, V2, and IT-during free viewing, focusing on the relationship between spiking activity, the order of fixations, and the fixated objects. We found that the population activity for individual objects became distinct across repeated fixations. These results suggest that neurons change their population activity depending on sensory experiences and thus raises a question about how visual sensory neurons shape their selectivity.