Low-Frequency Oscillations Arising From Competitive Interactions Between Visual Stimuli in Macaque Inferotemporal Cortex

Some neurons in the inferotemporal cortex (IT) of the macaque monkey respond to visual stimuli by firing action potentials in a series of sharply defined bursts at a frequency of about 5 Hz. The aim of the present study was to test the hypothesis that the oscillatory responses of these neurons depend on competitive interactions with other neurons selective for different stimuli. To test this hypothesis, we monitored responses to probe images displayed in the presence of other already visible backdrop images. Two stimuli were used in testing each neuron: a foveal image that, when displayed alone, elicited an excitatory response (the "object") and a peripheral image that, when displayed alone, elicited little or no activity (the "flanker"). We assessed the results of presenting these images separately and together in monkeys trained to maintain central fixation. Two novel phenomena emerged. First, displaying the object in the presence of the flanker enhanced the strength of the oscillatory component of the response to the object. This effect varied in strength across task contexts and may have depended on the monkey's allocating attention to the flanker. Second, displaying the flanker in the presence of the object gave rise to sometimes strong oscillations in which the initial phase was negative. This was all the more striking because the flanker by itself elicited little or no response. This effect was robust and invariant across task contexts. These results can be accounted for by competition between two neuronal populations, one selective for the object and the other for the flanker, if it is assumed that the visual responses of each population are subject to fatigue.