Attention to Features Precedes Attention to Locations in Visual Search: Evidence from Electromagnetic Brain Responses in Humans

Abstract

Single-unit recordings in macaque extrastriate cortex have shown that attentional selection of nonspatial features can operate in a location-independent manner. Here, we investigated analogous neural correlates at the neural population level in human observers by using simultaneous event-related potential (ERP) and event-related magnetic field (ERMF) recordings. The goals were to determine (1) whether task-relevant features are selected before attention is allocated to the location of the target, and (2) whether this selection reflects the locations of the relevant features. A visual search task was used in which the spatial distribution of nontarget items with attended feature values was varied independently of the location of the target. The presence of task-relevant features in a given location led to a change in ERP/ERMF activity beginning ϳ140 msec after stimulus onset, with a neural origin in the ventral occipito-temporal cortex. This effect was independent of the location of the actual target. This effect was followed by lateralized activity reflecting the allocation of attention to the location of the target (the well known N2pc component), which began at ϳ170 msec poststimulus. Current source localization indicated that the allocation of attention to the location of the target originated in more anterior regions of occipito-temporal cortex anterior than the feature-related effects. These findings suggest that target detection in visual search begins with the detection of task-relevant features, which then allows spatial attention to be allocated to the location of a likely target, which in turn allows the target to be positively identified.

The neural basis of attentional control in visual search

“…The transition from guidance to selection is therefore marked by the transition from feature-selective activation patterns that are triggered in a spatially global fashion across the visual field to spatially specific modulations of neural responses to potentially task-relevant objects. In contrast to the common assumption that spatial attention is generally faster than attention for features [37,38], feature-based attention should precede spatial attention during visual search when the location of target objects is not known in advance [39].…”

“…The N2pc is an enhanced negativity at posterior electrodes contralateral to candidate target objects in visual search displays [46,47]. This component is generated during the spatially selective enhancement of target processing in ventral visual cortex [39], which is controlled by recurrent signals from higherlevel attentional control areas such as FEF [48]. Because it tracks the operation of selective attention on a millisecond-by-millisecond basis, the N2pc can provide unique insights into the time course of attentional object selection in visual search (Box 3 and Figure 4).…”

The gradual emergence of spatially selective target processing in visual search: From feature-specific to object-based attentional control.

“…However, previous ERP experiments have reported effects of feature-based attention at post-stimulus latencies of 100 ms (Zhang & Luck, 2009) or 140 ms (Hopf, Boelmans, Schoenfeld, Luck, & Heinze, 2004), well before the typical onset of the N2pc component, suggesting that feature-based attention modulates early feedforward stages in the visual processing hierarchy (e.g., Zhang & Luck, 2009). In contrast, the N2pc is assumed to be generated at a subsequent stage where spatially selective processing is triggered by recurrent feedback that signals the presence of target-matching features which are detected during the rapid feedforward analysis of visual information (e.g., Luck & Hillyard, 1994).…”

EPS Mid-Career Award 2014

“…In fact, the pattern of N2pc results observed in our recent studies where different objects with target-matching features were presented simultaneously or in rapid succession (Eimer & Grubert, 2014a, 2014bGrubert & Eimer, 2015) appears to be similar to the spatially global modulations of visual processing produced by feature-based attention that were described in the previous section as the neural correlate of attentional guidance. Although such feature-based attention effects typically emerge earlier than the N2pc component (e.g., Hopf et al, 2004;Zhang & Luck, 2009), the question remains whether the N2pc results discussed earlier reflect spatially global feature-based attentional guidance or parallel space-based attentional selection processes. This question assumes that there is a strict separation between spatially global guidance processes (feature-based attention) and spatially specific selection mechanisms (spatial attention), and that this dichotomy describes functionally and temporally discrete stages of attentional processing during visual search.…”