Simultaneous selection by object-based attention in visual and frontal cortex

Abstract

Models of visual attention hold that top-down signals from frontal cortex influence information processing in visual cortex. It is unknown whether situations exist in which visual cortex actively participates in attentional selection. To investigate this question, we simultaneously recorded neuronal activity in the frontal eye fields (FEF) and primary visual cortex (V1) during a curve-tracing task in which attention shifts are object-based. We found that accurate performance was associated with similar latencies of attentional selection in both areas and that the latency in both areas increased if the task was made more difficult. The amplitude of the attentional signals in V1 saturated early during a trial, whereas these selection signals kept increasing for a longer time in FEF, until the moment of an eye movement, as if FEF integrated attentional signals present in early visual cortex. In erroneous trials, we observed an interareal latency difference because FEF selected the wrong curve before V1 and imposed its erroneous decision onto visual cortex. The neuronal activity in visual and frontal cortices was correlated across trials, and this trial-to-trial coupling was strongest for the attended curve. These results imply that selective attention relies on reciprocal interactions within a large network of areas that includes V1 and FEF.contour grouping | noise correlation | error trials V isual scenes are usually too complex for all information to be analyzed at once. Selective attention selects a subset of the objects in the visual scene for detailed analysis at the expense of other items. Visual objects compete for selection, and the outcome of this competition depends on bottom-up cues such as saliency and perceptual organization and top-down cues that signal the objects' behavioral relevance (1). It is not well understood how these different cues interact and which brain areas take the lead in visual selection.The top-down mechanisms for attentional selection are tightly linked to those for the selection of actions (2), and accordingly, cortical areas related to action planning influence the deployment of visual attention. The frontal eye fields (FEF) is one such area that is involved in visual processing, shifts of visual attention (2, 3), and also in the control of eye movements (4, 5). Area FEF contains different types of cells. Visual processing relies on visual and visuomovement cells, whereas the programming of eye movements relies on the activity of visuomovement and movement cells (6, 7). There are several lines of evidence that also implicate FEF in attentional control. First, FEF inactivation impairs attention shifts toward the contralateral visual field (8, 9). Second, subthreshold FEF microstimulation enhances neuronal activity in visual cortex in a manner that is reminiscent of selective attention (10, 11). Third, a role of FEF in the top-down guidance of attention is supported by studies on visual search. In search, selection signals in frontal cortex precede those in area V4 by 50 ms, sugges...

Belief states as a framework to explain extra-retinal influences in visual cortex

“…If the monkeys made an error and chose the wrong curve, the erroneously selected curve elicited extra activity, both in V1 and in the frontal eye fields. However, now selection in frontal cortex preceded selection in visual cortex as if the frontal cortex imposed its erroneous decision onto visual cortex [13 ]. In addition, the authors observed correlations between frontal and visual cortex that were strongest for the attended curve.…”

“…One example task associated with attention shifts is curve-tracing ( [13 ], Figure 1b). The authors of this study required monkeys to mentally trace a curve that starts at a fixation point to determine the endpoint of this curve, because the circle at the end was the target for an eye movement.…”

“…The green square in the left panels illustrates the location of a receptive field in V1; the green ellipse denotes a receptive field in FEF. Reproduced with permission from[13 ]. (c) Simultaneous recordings in left and right V4 (2 Â 48 contacts) while monkeys had to detect small changes in the orientation in a stream of successively presented pairs of grating stimuli.…”

Visuomotor Functions in the Frontal Lobe

“…Most of these studies have focused on the FEF and areas in the back of the brain, and the task design and measurement method used vary widely from study to study. Every study has found that when the target is more difficult to locate, neurons in the FEF and in the dorsolateral PFC (dlPFC) signal its location either before or as early as neurons in occipital, parietal, and temporal areas do , Cohen et al 2009a, Monosov et al 2010, Zhou & Desimone 2011, Gregoriou et al 2012, Ibos et al 2013, Pooresmaeili et al 2014). This conclusion is based on chronological comparison of not only single-unit modulation times but also intracortical local field potentials and the N2pc event-related potential (ERP), which is identified with the allocation of visual attention .…”

Paying Attention to the Cortical Layers

“…First, studies have consistently shown that attention increases the spike rates of neurons encoding attended stimuli compared to non-attended stimuli (Desimone and Duncan, 1995). The effect on firing rates has been observed in many, if not all, areas of the cerebral cortex, ranging from primary visual cortex to areas of the frontal cortex (Pooresmaeili et al, 2014). Second, attention makes neural responses more reliable.…”