Right temporoparietal junction activation by a salient contextual cue facilitates target discrimination
Research Highlights
►Presence of a salient contextual cue increases R TPJ connectivity with attention and decision areas. ►R TPJ is sensitive to contextual sensory information that facilitates behavior. ►L TPJ responds to a salient contextual cue only when it co-occurs with a target..
Introduction
In order to behave efficiently in a complex environment, it is necessary to not only direct top-down attention to task-relevant information, but also to integrate sensory events of contextual relevance. Contextual information may not always provide sufficient information to immediately execute goal-relevant actions, but may nevertheless predict the occurrence of events and behaviors related to the current goal. Successful use of such contextual information requires the rapid integration of previously unattended stimuli with ongoing top-down selection processes. In this study, we explored the role of TPJ in representing contextual information that could be used to bias mechanisms of top-down information selection.
The right temporoparietal junction (R TPJ) has consistently been found to be activated by unexpected stimulus events of behavioral relevance. Behavioral relevance has typically been defined by task-relevant target properties. For example, in variations of the Posner cueing paradigm (Posner, 1980), R TPJ and the right inferior frontal gyrus (IFG) were activated specifically by “invalid” targets that appeared in an unexpected location (e.g. Corbetta et al., 2000, Corbetta et al., 2008, Indovina and Macaluso, 2007, Kincade et al., 2005, Natale et al., 2010, Shulman et al., 2007, Vossel et al., 2009). Similarly, R TPJ is sensitive to non-targets that share the target color (Hu et al., 2009, Natale et al., 2010, Serences et al., 2005) or category (Hampshire et al., 2007), and task cues that indicate a new target location (Shulman et al., 2009). Unexpected stimuli in these paradigms produced shifts in spatial attention, but shifts of attention are not a necessary condition for R TPJ activation: R TPJ also responds to oddball targets within an attended stream (Marois et al., 2000), cues indicating low frequency target locations (Shulman et al., 2009) and sudden changes in continuous sensory events that violate expectations (Downar et al., 2000, Downar et al., 2002). While some of these studies also report left TPJ activation under similar conditions, R TPJ activation is generally more robust and reliable. R TPJ activation is stimulus-driven, but only in response to unexpected stimuli of potential behavioral relevance. This has led to the hypothesis that R TPJ and the ventral attentional network acts as a filter that selectively gates stimulus information based on task goals (Corbetta et al., 2008, Shulman et al., 2007).
In contrast, stimulus-driven attentional capture by perceptually salient stimuli that are completely task-irrelevant do not activate R TPJ. Instead, salient stimuli of this kind tend to interfere with task processing and activate the intraparietal sulcus (IPS) and frontal eye fields (FEF) (e.g. Corbetta et al., 2008, Indovina and Macaluso, 2007, Kincade et al., 2005). IPS and FEF form a dorsal attentional network that is thought to reflect the current distribution of spatial attention across the visual field (e.g., Bisley and Goldberg, 2003, Goldberg et al., 2006, Gottlieb, 2007), and to control the voluntary orientation of attention (e.g. Corbetta, 1998, Corbetta et al., 2000, Geng et al., 2006, Serences and Yantis, 2007, Yantis et al., 2002). Sensory stimuli that are completely irrelevant to current goals but yet capture attention are represented within the dorsal attentional priority map, and do not engage R TPJ and the ventral attentional network (e.g., Geng and Mangun, 2009).
These previous studies suggest that the mechanisms of stimulus-driven attention depend on the task-relevance of the stimulus. TPJ and the ventral attentional network are selectively activated by unexpected task-relevant stimuli, but task-relevance has so far been defined primarily by information that is directly related to target processing (e.g., targets, non-targets with target features, or target-related cues). Thus, while it has been hypothesized that TPJ is sensitive generally to any behaviorally relevant stimulus that leads to a change in the focus of attention, current studies have not addressed whether or not TPJ is sensitive to non-target contextual information that may facilitate the current behavioral goal.
In this study, we define task-relevance flexibly by manipulating the statistical relationship between a perceptually salient contextual cue and the appearance of a target stimulus. The contextual cue and target appeared in opposite visual fields within bilateral streams of “standard” stimuli (see Fig. 1). The contextual cue was only partially predictive of the appearance of the target, which allowed us to dissociate responses to the target alone, the salient contextual cue alone, and the coincidence of the two. The salient stimulus was therefore always of potential behavioral relevance, but only sometimes paired with a target. This allowed us to dissociate activation related to the detection of the potentially informative stimulus and its actual task-relevance.
Section snippets
Subjects
Imaging and behavioral data were collected from 16 subjects (8 females, 1 left handed). Three were excluded based on technical problems with data acquisition or excessive head motion; data from 13 subjects were entered into our analyses. All were screened for MRI compatibility and gave written informed consent in accord with the local ethics clearance as approved by NIH. All had normal or corrected-to-normal vision and none had a history of neurological or psychiatric disorder.
Experimental design
A factorial
Eye-tracking
Eye data were acquired from 9 out of the 13 subjects whose fMRI data were included for analysis. Data quality from 4 out of 13 was inadequate for analysis. Data from each subject were divided into the twelve experimental conditions given by crossing the attended side (left and right), target difficulty (easy and hard), and the three target plus contextual cue conditions of interest (target + contextual cue, target alone and contextual cue alone). The distribution of fixation points in each
Discussion
The temporoparietal region is thought to be a critical hub within the ventral attentional control network that supports the detection of behaviorally relevant stimuli. This is in contrast to the dorsal attentional network (including IPS and FEF), which contain attentional priority maps that reflect the current distribution of attention amongst all stimuli, regardless of task-relevance (e.g., Balan and Gottlieb, 2006, Bisley and Goldberg, 2003, Donner et al., 2002, Geng and Mangun, 2009,
Acknowledgments
This work was supported by grants from NIMH (MH055714) and NEI (EY015387). We would like to thank Pia Rotshtein and two anonymous reviewers for their many helpful comments on the manuscript.
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