Saliency affects feedforward more than feedback processing in early visual cortex

Highlights

• Saliency affects visual suppression at feedforward more than feedback processing stages in early visual cortex.

• Red is inherently more salient than other hues regardless of luminance and saturation.

• Task discrimination difficulty does not affect TMS-induced visual suppression.

Abstract

Early visual cortex activity is influenced by both bottom-up and top-down factors. To investigate the influences of bottom-up (saliency) and top-down (task) factors on different stages of visual processing, we used transcranial magnetic stimulation (TMS) of areas V1/V2 to induce visual suppression at varying temporal intervals. Subjects were asked to detect and discriminate the color or the orientation of briefly-presented small lines that varied on color saliency based on color contrast with the surround. Regardless of task, color saliency modulated the magnitude of TMS-induced visual suppression, especially at earlier temporal processing intervals that reflect the feedforward stage of visual processing in V1/V2. In a second experiment we found that our color saliency effects were also influenced by an inherent advantage of the color red relative to other hues and that color discrimination difficulty did not affect visual suppression. These results support the notion that early visual processing is stimulus driven and that feedforward and feedback processing encode different types of information about visual scenes. They further suggest that certain hues can be prioritized over others within our visual systems by being more robustly represented during early temporal processing intervals.

Introduction

It has been known for nearly a century that early visual cortex is crucial for vision in humans, with lesions to this region producing stereotypical visual field deficits (Holmes, 1918). Furthermore, neurons within areas V1 and V2 in early visual cortex have been shown to produce highly specific and consistent responses to visual information, such as edges and orientations, even in anesthetized animals (Hubel and Wiesel, 1968, Livingstone and Hubel, 1988). Based on these long-standing observations, it had originally been assumed that visual information processing in V1/V2 proceeds automatically and independently from bottom-up and top-down factors, such as stimulus feature saliency (differences in hue, size, etc.) and attentional set (attention to certain features, locations, temporal intervals, sensory modalities, etc.).

However, several studies have shown that V1/V2 does not only serve as a passive relay of information to higher-order areas, but instead amplifies responses to salient bottom-up information (Li, 1999, Li et al., 2006), is involved beyond the initial stages of visual information processing via feedback loops (Lamme & Roelfsema, 2000), and is influenced by top-down factors such as attention (Motter, 1993, Somers et al., 1999) and task (Huk & Heeger, 2000). The time course of these bottom-up and top-down influences, nevertheless, remains unclear. For example, some evidence suggests that bottom-up factors, such as saliency, should influence processing in V1 at early temporal intervals (for a review see Theeuwes, 2010), whereas top-down factors, such as attentional set, should affect later processing. Other evidence, however, suggests that attention may influence early neuronal responses in V1 (Ito & Gilbert, 1999) and that saliency maps are generated in the posterior parietal cortex after initial processing (Gottlieb, Kusunoki, & Goldberg 1998; but see Zhang, Zhaoping, Zhou, & Fang 2012).

In the current study we manipulated bottom-up feature saliency as well as top-down attentional set to investigate how these variables affect early visual cortex activity at different time intervals. We applied TMS over V1/V2 at varying temporal intervals after stimulus onset to assess whether the magnitude of visual suppression (Amassian et al., 1989, Kammer, 2007) was affected by saliency and attentional set. If bottom-up saliency differences influence processing in V1/V2 only at early temporal intervals, then we should find that TMS at early temporal intervals produces different magnitudes of suppression based on stimulus feature saliency, regardless of attentional set. Furthermore, if top-down attentional set differences influence processing in V1/V2 only at later temporal intervals, then we should find that TMS at later temporal intervals produces different magnitudes of suppression based on attentional set, regardless of feature saliency differences.