Visual looming and receding networks in awake marmosets investigated with fMRI

Abstract

An object that is looming toward a subject or receding away contains important information for determining if this object is dangerous, beneficial or harmless to them. This information (motion, direction, identity, time-to-collision, size, velocity) is analyzed by the brain in order to execute the appropriate behavioral responses depending on the context: fleeing, freezing, grasping, eating, exploring. In the current study, we performed ultra-high-field functional MRI (fMRI) in awake marmosets to explore the patterns of brain activation elicited by visual stimuli looming toward or receding away from the monkey. We found that looming and receding visual stimuli both activate a large cortical network in frontal, parietal, temporal and occipital cortex in areas involved in the analysis of motion, shape, identity and features of the objects. Looming stimuli strongly activated a network composed of the pulvinar, superior colliculus, prefrontal cortex and temporal cortical areas. This may underlie the existence of an alert network that processes the visual stimuli looming toward their peripersonal space by extracting the crucial information brought by the stimulus and evaluating its potential consequences to the observer. We hypothesize that this network is involved in the planning of protective behaviors (e.g. fleeing or freezing) and in emotional reaction (e.g. anxiety, fear). These findings support the view that this network is preserved through evolution and that the marmoset is a viable model to study visual and multisensory processes by using fMRI to guide further invasive recordings and/or pharmacological manipulations.\n\nSignificant statementAn object that is looming toward a subject or receding away contains important information for determining if this object is dangerous, beneficial or harmless to them. Here, we identified the functional network in non-human primates that was activated by visual stimuli looming toward or away from the animals using ultra-high-field functional magnetic resonance imaging. Our findings show that large cortical activations are elicited by both looming and receding visual conditions. However, some activations were specific to the looming condition, suggesting that the integration of cues in the looming direction rely on strong connections between cortical and subcortical areas, which allows primates to react properly for protecting themselves against a potential threat.