Stimulus context modulates competition in human extrastriate cortex

Abstract

When multiple stimuli appear simultaneously in the visual field, they are not processed independently, but interact in a mutually suppressive way suggesting that they compete for neural representation in visual cortex. The biased competition model of selective attention predicts that the competition can be influenced by both top-down and bottom-up mechanisms. Directed attention has been shown to bias competition in favor of the attended stimulus in extrastriate cortex. Here, we show that suppressive interactions among multiple stimuli are eliminated in extrastriate cortex when they are presented in the context of pop-out displays, in which a single item differs from the others, but not in heterogeneous displays, in which all items differ from each other. The pop-out effects appeared to originate in early visual cortex and were independent of attentional top-down control suggesting that stimulus context may provide a powerful influence on neural competition in human visual cortex.Natural visual scenes are cluttered and contain many different objects that cannot all be processed at once due to limited processing capacity of the visual system 1 , suggesting that multiple objects present at the same time in the visual field compete for neural representation 2-3 . Neural correlates for competitive interactions among multiple stimuli have been found in visual cortex in single-cell physiology and functional brain imaging studies, showing that multiple stimuli presented in nearby locations are not processed independently from each other but interact in a mutually suppressive way 4-8 . These sensory suppressive interactions occur most strongly at the level of the receptive field (RF) 5,9 and are therefore prominent in extrastriate areas where RFs are large enough to encompass multiple stimuli 4-8 .According to the "biased competition model" of selective attention 2-3,11 , competition among multiple stimuli can be influenced both by means of top-down processes related to the selection of information that is relevant to current behavioral goals and by bottom-up, stimulus driven processes. For example, if one directs attention to a particular location in a cluttered scene, processing of information at the attended location will be facilitated and processing of unwanted information from nearby distracters will be suppressed 12 , suggesting that competition is biased in favor of the attended stimulus. On the other hand, if a salient stimulus is present in a cluttered scene, it will be effortlessly and quickly detected independent of the number of distracters 13 , suggesting that competition is biased in favor of the salient stimulus. At the neural level, evidence in support of the biased competition model was found in studies showing that spatially directing attention to one of multiple stimuli eliminates or reduces the suppressive influences of nearby stimuli in extrastriate cortical areas, consistent with the idea that selective attention biases the competition among multiple stimuli in favor of the attended stimulus by cou...

Neural evidence for competition-mediated suppression in the perception of a single object

“…The task was designed to be difficult in order to keep participants focused on fixation; the RSVP stream was fast (4 Hz), continuous throughout the entire experiment, and small in size (0.5 o of visual angle). Thus, we expected low accuracy, and our participants' accuracy was even lower than in previous studies using this task (e.g., Beck & Kastner, 2005;, as we did not provide training or practice trials beforehand as others did.…”

“…To assay competition in the perception of a single object, we adapted an fMRI design similar to that used by others to measure competitive suppression between objects (e.g., Beck & Kastner, 2005;Scalf, Basak & Beck, 2011). Participants performed a demanding rapid serial visual presentation (RSVP) task at fixation while the silhouettes appeared individually in either the upper right visual field (RVF) or the upper left visual field (LVF).…”

“…Using lateralized presentations allowed us to accurately locate representations in visual cortex of the contralateral hemisphere. Previously published fMRI studies have presented competing stimuli to the RVF only and assessed left hemisphere (LH) activation only (e.g., Beck & Kastner, 2005;Scalf et al, 2011). Thus, we expected to observe evidence of competition-mediated ground suppression in the LH when we presented our silhouettes in the RVF, but we were uncertain whether we would observe evidence of competition-mediated ground suppression in the right hemisphere (RH) when we presented our silhouettes in the LVF, especially given that our stimuli are so different from those previously used.…”

“…11 attention is focused on fixation (cf. Beck & Kastner, 2005;Scalf, Basak & Beck, 2011). 1 We used it for the same purpose.…”

“…Competition-mediated suppression between multiple objects has been observed in visual areas as low as V1/V2 and as high as the inferior temporal cortex (IT) via single-cell recording in monkeys (Miller et al, 1993;Reynolds et al, 1999) and functional magnetic resonance imaging (fMRI) in humans (Beck & Kastner, 2005;Kastner, De Weerd, Desimone, & Ungerleider, 1998;Scalf & Beck, 2010;see Beck & Kastner, 2009, for a review).…”