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Dissociating the Neural Mechanisms of Visual Attention in Change Detection Using Functional MRI

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Dissociating the Neural Mechanisms of Visual Attention in Change Detection Using Functional MRI Dissociating the Neural Mechanisms of Visual Attention in Change Detection Using Functional MRI Scott A. Huettel, Gu¨ven Gu¨zeldere, and Gregory McCarthy Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/13/7/1006/1759185/089892901753165908.pdf by guest on 18 May 2021 Abstract & We investigated using functional magnetic resonance ventral visual areas was temporally associated with the imaging (fMRI) the neural processes associated with perform- duration of visual search. As such, our results support a ance of a change-detection task. In this task, two versions of distinction between brain regions whose activation is modu- the same picture are presented in alternation, separated by a lated by attentional demands of the visual task (extrastriate brief mask interval. Even when the two pictures greatly differ cortex) and those that are not affected by it (primary visual (e.g., as when a building is in different locations), subjects cortex). A second network of areas including central sulcus, report that identification of the change is difficult and often insular, and inferior frontal cortical areas, along with the take 30 or more seconds to identify the change. This thalamus and basal ganglia, showed phasic activation tied to phenomenon of ‘‘change blindness’’ provides a powerful and the execution of responses. Finally, parietal and frontal regions novel paradigm for segregating components of visual attention showed systematic deactivations during task performance, using fMRI that can otherwise be confounded in short-duration consistent with previous reports that these regions may be tasks. By using a response-contingent event-related analysis associated with nontask semantic processing. We conclude technique, we successfully dissociated brain regions associated that detection of change, when transient visual cues are not with different processing components of a visual change- present, requires activation of extrastriate visual regions and detection task. Activation in the calcarine cortex was associated frontal regions responsible for eye movements. These results with task onset, but did not vary with the duration of visual suggest that studies of change blindness can inform under- search. In contrast, the pattern of activation in dorsal and standing of more general attentional processing. & INTRODUCTION One challenge considered by recent functional neuro- Visual attention allows organisms to allocate processing imaging studies is the dissociation of different compo- resources to selected locations or objects in the visual nents of visual attention, such as cue-directed attention field. Lesion studies in humans and nonhuman primates versus target responses (Hopfinger, Buonocore, & Man- have suggested that visual attention depends upon a gun, 2000) or orienting to locations versus detection of distributed network of brain regions, including the stimuli in unattended locations (Corbetta, Kincade, Ol- posterior parietal cortex (Posner, Walker, Friedrich, & linger, McAvoy, & Shulman, 2000). In the present study, Rafal, 1984; Mesulam, 1981), frontal cortex (Paus, 1996), our goal was to dissociate, in a single experimental task, and cingulate cortex, as well as the superior colliculus brain regions associated with attentional processing and thalamus (Posner & Petersen, 1990). In conjunction, from those associated with other components of the functional neuroimaging studies have demonstrated the task, such as nonattentive perceptual processing or participation of the intraparietal sulcus (IPS), posterior response execution. We employed a change detection superior frontal gyrus (SFG), and precentral gyrus in paradigm known as a ‘‘flicker’’ task (Rensink, O’Regan, visual attention tasks (Courtney, Petit, Maisog, Unger- & Clark, 1997; Rensink, 2000b) while testing subjects leider, & Haxby, 1998; Nobre et al., 1997; Corbetta, using functional magnetic resonance imaging (fMRI). On Miezen, Shulman, & Petersen, 1993; Corbetta, Shulman, each trial, two photographs were presented in alterna- Miezin, & Petersen, 1995). This network may also in- tion, separated by a short-duration mask. The images clude visual cortical regions, depending upon the stimuli differed in one aspect, such as the presence/absence, and task (e.g., Corbetta, Miezen, Dobmeyer, Shulman, & color, or position of a single object. The subject’s task Petersen, 1990), in line with the distinction between was to identify the change. Figure 1 provides an example ventral and dorsal visual pathways (Ungerleider & Mis- of an image pair used in the current experiment. The hkin, 1982; Ungerleider & Haxby, 1994). two photographs in the pair differ in that a sign in the upper right above the building is present in the left image but absent in the right image. The short-duration Duke University, Durham, NC mask prevented automatic detection of change that D 2001 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 13:7, pp. 1006–1018 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892901753165908 by guest on 24 September 2021 Figure 1. The flicker task used in the present experiment. Shown in A is an example stimulus pair from the current experiments. These two scenes differ in one aspect, the pre- sence or absence of a sign at upper right. Typical changes across scenes were the pre- sence/absence of an object, the location of an object, or the color of an object. The order of Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/13/7/1006/1759185/089892901753165908.pdf by guest on 18 May 2021 events on any one trial is shown in B. Between each pair of trials was a 2-sec fixation cross on a black screen. For the first 30 sec of each trial, the pictures were presented in alternation, each for 300 msec with a 100-msec grayscale mask between them. During the final 10 sec of each trial, the mask was removed and the pictures were presented for 400 msec. occurs when low-level motion transients are available, sees the same images and mask flickering at a constant such as when the interval between stimuli is less than rate, with no interruptions from cuing, extended inter- about 80 msec (Pashler, 1988; Phillips, 1974). Behavioral stimulus interval, or feedback. Differences in the pattern evidence suggests that, when this automatic detection of activation over time may therefore be attributed to process is not available, subjects engage in a controlled cognitive processing and not to stimulus presentation. serial search among display elements (Rensink et al., Despite these characteristics and the significant recent 1997). The search process is guided by the semantic interest in behavioral studies of change detection (e.g., content of the image, such that changes are more Rensink, 2000a; Simons & Levin, 1997), functional neu- quickly detected on objects that are named in verbal roimaging studies of change detection in a flicker task descriptions (Rensink et al., 1997). As such, cuing has have not been previously conducted. relatively little effect on search, with facilitation only The subject’s behavioral response in a change-detec- reported for color changes (Aginsky & Tarr, 2000). tion task provides an objective marker for the subjective Finally, detection of change is associated with the locus process of visual search. Taking advantage of this, we of attention rather than of eye position, although the developed an analysis technique that uses response- two move similarly: Even when looking right at the contingent event-related fMRI. Because of the extended change location, subjects fail to detect 40% of changes duration of our experimental task, we can use informa- across blinks (O’Regan, Deubel, Clark, & Rensink, tion about the duration and timing of responses to guide 2000). analyses. Typical short-duration visual search tasks do Change-detection tasks of this kind have two charac- not temporally separate search and response processes teristics that map well onto fMRI analysis techniques. by durations greater than the temporal resolution of the First, change detection is a slow process in comparison fMRI hemodynamic response. Furthermore, there is to other visual searches (hence the name, ‘‘change little variability in the duration of the search process blindness’’). Response times in masked change-detec- (e.g., from 1 to 2 sec). Our analysis uses the response- tion tasks typically range from 5 to 40 sec or more, time variability over trials to identify voxels whose depending on the scene characteristics. In the present activity is associated with visual search. Simply put, the study, mean response time was approximately 23 sec. In duration of voxel activation, if that voxel is associated contrast, most visual search tasks used in cognitive with search, should show sustained activation through- experiments have response times that are roughly one out search, with short-duration activation when the order of magnitude faster. Thus, the extended durations target is found quickly and long-duration activation of change-detection trials match well the temporal when the target is found slowly. In contrast, voxels properties of the fMRI hemodynamic response, which associated with low-level visual processing should only rises and falls over a minimum of 10–15 sec. A second show phasic activation at trial onset, due to the stimulus characteristic is display homogeneity, in that the raw appearance. Voxels associated with response processing visual stimulus has a constant pattern over an extended should show a hemodynamic response time-locked
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