Three-stage processing of category and variation information by entangled interactive mechanisms of peri-occipital and peri-frontal cortices

Hamid Karimi-Rouzbahani

doi:10.1038/s41598-018-30601-8

Abstract

Object recognition has been a central question in human vision research. The general consensus is that the ventral and dorsal visual streams are the major processing pathways undertaking objects’ category and variation processing. This overlooks mounting evidence supporting the role of peri-frontal areas in category processing. Yet, many aspects of visual processing in peri-frontal areas have remained unattended including whether these areas play role only during active recognition and whether they interact with lower visual areas or process information independently. To address these questions, subjects were presented with a set of variation-controlled object images while their EEG were recorded. Considerable amounts of category and variation information were decodable from occipital, parietal, temporal and prefrontal electrodes. Using information-selectivity indices, phase and Granger causality analyses, three processing stages were identified showing distinct directions of information transaction between peri-frontal and peri-occipital areas suggesting their parallel yet interactive role in visual processing. A brain-plausible model supported the possibility of interactive mechanisms in peri-occipital and peri-frontal areas. These findings, while promoting the role of prefrontal areas in object recognition, extend their contributions from active recognition, in which peri-frontal to peri-occipital pathways are activated by higher cognitive processes, to the general sensory-driven object and variation processing.

Highlights

Humans can recognize the categories of objects in fractions of a second with remarkable accuracy[1,2]
The ventral stream starts from V1 and ends up at anterior inferior temporal cortex (IT)[7,8] and the dorsal stream starts from V1 and continues to parietal and areas in middle temporal cortices[9,10,11]
The spatiotemporal dynamics of category encoding was drastically different from those reported in Bar et al.[14]: the results showed the domination of feed-forward information flow from peri-occipital to peri-frontal areas in early processing time windows and the domination of feedback flows in the following time windows

Summary

Introduction

Humans can recognize the categories of objects in fractions of a second with remarkable accuracy[1,2]. Linearly-separable representations of objects as well as other accompanying aspects of information, which are processed by the layers of the two visual streams, are sent to the prefrontal cortex for final classification of representations into distinct categories[12] (e.g. categories of objects, movement directions, etc.) This view has been challenged by recent studies which observed category-related information in frontal brain areas, even earlier than they generally appeared in occipital and temporal brain areas after stimulus presentation[13,14,15]. Authors explained that the observed discrepancy from previous results (Bar et al.14) could have been explained by long stimulus presentation time (i.e. 500 ms) in their study which caused the domination of feed-forward information flow in early time windows[19] New paradigms, such as the one employed in the current study, which provides a shorter presentation time, are needed to reappraise the spatiotemporal transfer of category information between peri-occipital and peri-frontal brain areas

Objectives

Methods

Results