Fast ventral stream neural activity enables rapid visual categorization.

ABSTRACT

Primates can recognize objects embedded in complex natural scenes in a glimpse. Rapid categorization paradigms have been extensively used to study our core perceptual abilities when the visual system is forced to operate under strong time constraints. However, the neural underpinning of rapid categorization remains to be understood, and the incredible speed of sight has yet to be reconciled with modern ventral stream cortical theories of object recognition. Here we recorded multichannel subdural electrocorticogram (ECoG) signals from intermediate areas (V4/PIT) of the ventral stream of the visual cortex while monkeys were actively engaged in a rapid animal/non-animal categorization task. A traditional event-related potential (ERP) analysis revealed short visual latencies (<50-70ms) followed by a rapidly developing visual selectivity (within ~20-30ms) for most electrodes. A multi-variate pattern analysis (MVPA) technique further confirmed that reliable animal/non-animal category information was possible from this initial ventral stream neural activity (within ~90-100ms). Furthermore, this early category-selective neural activity was (a) unaffected by the presentation of a backward (pattern) mask, (b) generalized to novel (unfamiliar) stimuli and (c) co-varied with behavioral responses (both accuracy and reaction times). Despite the strong prevalence of task-related information on the neural signal, task-irrelevant visual information could still be decoded independently of monkey behavior. Monkey behavioral responses were also found to correlate significantly with human behavioral responses for the same set of stimuli. Together, the present study establishes that rapid ventral stream neural activity induces a visually selective signal subsequently used to drive rapid visual categorization and that this visual strategy may be shared between human and non-human primates.