Separable responses to error, ambiguity, and reaction time in cingulo-opercular task control regions

Highlights

• We examined responses to errors, ambiguity, and reaction time during two tasks.

• Reaction times were longer for ambiguous and error trials than clear trials.

• There were error > ambiguous > clear responses in cingulo-opercular regions.

• These effects remained when reaction time was regressed out.

• Cingulo-opercular responses represent multiple performance feedback processes.

Abstract

The dorsal anterior cingulate (dACC), along with the closely affiliated anterior insula/frontal operculum, have been demonstrated to show three types of task control signals across a wide variety of tasks. One of these signals, a transient signal that is thought to represent performance feedback, shows greater activity to error than correct trials. Other work has found similar effects for uncertainty/ambiguity or conflict, though some argue that dACC activity is, instead, modulated primarily by other processes more reflected in reaction time. Here, we demonstrate that, rather than a single explanation, multiple information processing operations are crucial to characterizing the function of these brain regions, by comparing operations within a single paradigm. Participants performed two tasks in an fMRI experimental session: (1) deciding whether or not visually presented word pairs rhyme, and (2) rating auditorily presented single words as abstract or concrete. A pilot was used to identify ambiguous stimuli for both tasks (e.g., word pair: BASS/GRACE; single word: CHANGE). We found greater cingulo-opercular activity for errors and ambiguous trials than clear/correct trials, with a robust effect of reaction time. The effects of error and ambiguity remained when reaction time was regressed out, although the differences decreased. Further stepwise regression of response consensus (agreement across participants for each stimulus; a proxy for ambiguity) decreased differences between ambiguous and clear trials, but left error-related differences almost completely intact. These observations suggest that trial-wise responses in cingulo-opercular regions monitor multiple performance indices, including accuracy, ambiguity, and reaction time.

Introduction

Much of cognitive neuroimaging research begins from a search for a single explanation for processing within a specific cortical region. This approach has certainly been prevalent in the case of response in the dorsal anterior cingulate (dACC), which in the broad literature extends dorsal to the medial superior frontal cortex (dACC/msFC).

Many explanations for the trial-related responses in dACC/msFC have been offered. It has often been suggested that these responses are related to accuracy or error probability. For example, work in our own lab has shown that the dACC/msFC has demonstrated greater activity to errors than correct trials, across multiple tasks (Dosenbach et al., 2006, Dosenbach et al., 2007; see also Emeric et al., 2008, Ito et al., 2003). On the other hand, many studies have been interpreted to suggest that dACC/msFC activity is related to processes associated with decision uncertainty. In one line of work, the dACC/msFC appears to show responses to ambiguity in semantic (Thompson-Schill et al., 1997), visual motion (Sterzer et al., 2002), and face processing paradigms (Demos et al., 2004), as well as ambiguity in emotion (Neta et al., 2013). Similarly, the dACC/msFC has been widely thought to respond more in situations of conflict (Botvinick et al., 1999, Botvinick et al., 2001, Carter et al., 1998, MacLeod and MacDonald, 2000), particularly when the task requires a response relevant to that conflict (Milham et al., 2001). Indeed, many studies that have examined ambiguity and conflict have described them as a co-activation and/or selection among competing response options (Botvinick et al., 2001, Milham et al., 2001, Sterzer et al., 2002, Thompson-Schill et al., 1997; see Grinband et al., 2011). Still other research has shown that when reaction time is accounted for, some of these processing distinctions (error, conflict/ambiguity) appear minimal or absent (Grinband et al., 2011). This work argues that the cingulate region is associated with a process primarily modulated by reaction time (e.g., sustained attention, effort, working memory), with slower reaction times (i.e., more time on task) eliciting greater activity.

Much of the preceding work has also suggested a high degree of similarity in the activation of the bilateral anterior insula/frontal operculum (aI/fO) in many of these tasks. For example, this region shows a response similar to the dACC/msFC in response to error (Dosenbach et al., 2006), perceptual recognition (Ploran et al., 2007), and a wide variety of other manipulations of conflict, error, and uncertainty (e.g., Grinband et al., 2006, Nee et al., 2011, Wessel et al., 2012, Wheeler et al., 2008), as well as ambiguity (Demos et al., 2004, Neta et al., 2013, Sterzer et al., 2002, Thompson-Schill et al., 1997). Moreover, resting state functional connectivity shows strong and significant correlations between the bilateral aI/fO and dACC/msFC activity (Dosenbach et al., 2007), suggesting that they comprise the core of a larger “cingulo-opercular” system. Taken together, these effects provide further support for the notion that these regions, and their processing contributions, should be considered in concert.

Interestingly, the trial-related signals described here and in many other studies are not the only responses attributed to the cingulo-opercular regions. Mixed block/event-related designs (see Fig. 1) that can model both sustained and transient signals during a task have been used to demonstrate that these regions show three distinct task-control signals across a wide variety of tasks. In addition to transient, trial-related signals described above, which we associate with performance feedback, there is (2) a transient start signal at the beginning of a task block, which may include signals related to the loading of task parameters, and (3) a sustained signal across an entire task block, presumably related to task maintenance. Thus, among potential other processes, these regions are thought to be involved in controlling goal-directed behavior including the stable maintenance of task set (see Dosenbach et al., 2008 for a review). Therefore, we suggest that any trial-related effects that are attributed to these regions (e.g., error-related activity, conflict) should fit into a greater model of how these regions relate to task control. It should be noted that the cingulo-opercular network is not the only network attributed to task control (e.g., frontoparietal). Importantly, previous work has argued that the cingulo-opercular network is responsible for task control operations that are distinct from the frontoparietal network (Dosenbach et al., 2006, Dosenbach et al., 2007, Dosenbach et al., 2008). In particular, in the context of broad task control (which includes all three signals mentioned above), we have shown that the cingulo-opercular network might be more useful for stable task maintenance, whereas the frontoparietal network is more useful for online adaptive control. Moreover, we have found that the transient signals in the cingulo-opercular network come online at or near the end of the trial, suggesting that these responses serve as feedback into the task set, whereas the signals in the frontoparietal network effects begin early in the trial and may be more related to accumulating information over the course of the trial (Ploran et al., 2007). Further, the error-related signals in the frontoparietal regions and cingulo-opercular regions have different temporal characteristics (e.g., Wheeler et al., 2008). Because of these a priori reasons to believe that these networks represent distinct mechanisms of task control, we are motivated here to examine not the control signals of each mechanism, but rather we focus on the nature of the signals in cingulo-opercular regions, in particular as they are related to performance feedback.

Importantly, given that much of the preceding thought on cingulo-opercular regions has been directed at rationalizing a single explanation for error-related and uncertainty-related activity, a primary goal of the present work was to compare the neural signatures of trial-related responses in these regions (while also considering reaction time effects), in order to determine whether they are the result of one generic computation or, instead, resulting from multiple different computations. Moreover, we aim to demonstrate the generalizability of these effects across task contexts. To this end, we used two tasks in which there are both ambiguous and clear (i.e., unambiguous) trials, and in which participants also made errors. Specifically, we asked participants to make abstract/concrete judgments about English nouns (semantic task), as well as rhyming judgments about English word pairs (phonological task). We predict that, similarly for both tasks, there will be separable neural signatures for the three trial-related responses tested here: errors, uncertainty/ambiguity, and reaction time.