Habituation of Oculomotor Capture by Sudden Onsets: Stimulus Specificity, Spontaneous Recovery and Dishabituation

Previous studies have confirmed that visual onsets are very powerful in attracting our gaze. The reflexive saccades triggered by sudden onsets have a high adaptive value because they ensure a rapid inspection of potentially appetitive or dangerous events. Here we showed, however, that such exogenously driven saccades are rapidly attenuated as the exposure to the same irrelevant onset progresses. Crucially, we found that such decrement in oculomotor capture conforms to several key features of habituation, an ancestral and widespread form of learning, consisting in a response reduction to a repeated irrelevant stimulation. In addition, we documented both spontaneous recovery and specificity of habituation, the phenomenon of dishabituation, and that habituation of capture was stimulation-frequency dependent. We also found both short-term and long-term habituation of oculomotor capture. Although we cannot exclude the contribution of top-down strategic inhibitory mechanisms to filter the onset distractors, the oculomotor capture reduction that we have documented finds a straightforward explanation in the neural and cognitive mechanisms underlying habituation of the orienting reflex, as originally suggested by Sokolov. Our study lends support to the idea that habituation plays a key filtering role in regulating the exogenous saccadic response triggered by peripheral onset distractors. Public Significance Statement The capacity to overcome distraction is a key feature of a cognitive system that must ensure an efficient interaction with the surrounding environment, but the underlying psychological and neural mechanisms remain elusive. This study demonstrated that our brain can capitalize on habituation, an ancestral form of learning that we share with other subhuman animals, to learn to ignore the distracting stimulation. Specifically, we found that although initially our gaze is automatically attracted by the sudden occurrence of a new irrelevant stimulus in the visual field, with repeated exposure to the distractor the involuntary oculomotor capture is progressively attenuated. By showing that the reflexive saccadic response is subject to habituation, whose neurobiological mechanisms have been extensively studied with animal models, our study offers a new perspective to investigate the cognitive mechanisms that can counteract distraction.