From Coarse to Rich: Successive Waves of Visual Perception in Prefrontal Cortex

Abstract

The ventrolateral prefrontal cortex (vlPFC) is well known for its involvement in high-level functions such as cognitive control and language. However, vlPFCs role in visual processing is less clear. Here, we investigated how neuronal ensembles in the vlPFC dynamically encode different types of visual information. Using chronic recording of spiking activity, we investigated vlPFCs representational geometry in a macaque monkey passively viewing a large set of naturalistic images, and compared this to representations in deep neural networks (DNNs). We found that the vlPFC processes visual information in two stages. First, an "early" response from 50 to 90 ms after stimulus onset encodes the low spatial frequency component of an image. It contains sufficient information to form a coarse estimate of the position and category of a salient object. Then, from 100 ms on, the representational geometry changes and contains much richer information. This late period contains non-categorical information typically present in conscious experiences such as the orientation of a face and natural scenes in the background. The late window also enables sub-category identification, which is boosted by the low spatial category prior. These results suggest that the vlPFC has a dual role in natural vision: first forming fast low-spatial-frequency-based priors shaping feed-forward visual processing, and subsequently maintaining a detailed and rich representation of a visual scene. SignificanceWhat information does the prefrontal cortex represent during natural vision, and how does this relate to conscious experience? Theories of consciousness differ sharply on whether prefrontal activity reflects detailed perceptual content or only high-level, task-related information. Using dense neural recordings during passive viewing of thousands of naturalistic images, we show that the ventrolateral prefrontal cortex processes visual information in two distinct stages: an early, coarse estimate of the visual scene is followed by a richer, high-dimensional representation that includes sub-category identity and other perceptual details. These findings reveal that prefrontal circuits encode more of the content of visual experience than previously assumed, even in the absence of a task.