Neural mechanisms of goal-contingent task disengagement: Response-irrelevant stimuli activate the default mode network

Abstract

As we experience the world, we must decide not only when and how to act based on input from the environment, but also when to avoid responding in situations where acting could lead to a detrimental outcome. The ability to regulate behavior in this way requires flexible cognitive control, as the same stimulus may call for a response in one context but not in another. In this sense, explicit non-responding can be characterized as an active, goal-directed cognitive process. Little is known about the mechanisms by which a currently active goal state modulates information processing to support the avoidance of undesired responding. In the present study, participants executed or withheld responses to a color target based whether its color matched that of a cue at the beginning of each trial. Behavioral and neural responses to task-irrelevant stimuli appearing as distractors were examined as a function of their relationship to the currently response-relevant color indicated by the cue. We observed a robust pattern in which stimuli possessing the currently response-irrelevant feature activate the default mode network (DMN), which was associated with a behavioral cost on trials in which this stimulus competed with a response-relevant target. Our findings reveal a role for the DMN in goal-directed cognitive control, facilitating active disengagement based on contextually-specific task demands.

Introduction

The same stimulus may demand a response in one situation and the withholding of that response in another. For example, certain roadway intersections contain a stop sign that only applies to drivers intending to turn in a particular direction (e.g., stop except for right turn). In order to behave effectively, organisms must be able to flexibly modulate whether and how they respond to environmental input based on such contextually-specific demands. The coordination of information processing that supports goal-directed behavior in this way is broadly referred to as cognitive control.

Cognitive control is typically examined in the context of selecting and executing a response based on a set of currently relevant task rules (Badre and D'Esposito, 2007, Koechlin et al., 1999, Koechlin et al., 2000). Research using this approach highlights the important role of the prefrontal cortex (PFC) in flexibly configuring information processing to support goal-directed behavior (Badre and D'Esposito, 2007, Koechlin et al., 1999, Koechlin et al., 2000). The need to refrain from responding, however, may similarly require consideration of currently relevant task rules. Under such conditions, explicit non-responding can also be thought of as an active, goal-directed cognitive process.

The cancelation of a planned action has been investigated using the stop signal task, which implicates the inferior frontal and insular cortex and pre-supplementary motor area (pre-SMA) in response inhibition (e.g., Aron and Poldrack, 2006, Aron et al., 2003, Cai et al., 2014, Sharp et al., 2010). Similar findings have been observed using a simple go/no-go (GNG) task in which the no-go stimulus is consistent across trials (e.g., Liddle et al., 2001, Watanabe et al., 2002). More flexible and cognitively demanding response inhibition has also been investigated using a variant of the sustained attention to response (SART) task in which immediately repeated stimuli require the withholding of a prepotent response, which implicates additional areas of prefrontal cortex reflecting greater demand for cognitive control (e.g., Garavan et al., 1999, Garavan et al., 2003, Hester et al., 2004, Kelly et al., 2004, Simmonds et al., 2008).

In contrast to such overt response inhibition, less is known about the mechanisms by which cognitive control processes flexibly configure information processing to support the avoidance of responding in error. Contextually dependent response preparation and selection has been investigated using the AX variant of the continuous performance task (AX-CPT; e.g., Braver et al., 2001, Braver and Cohen, 2001, Paxton et al., 2008). In the AX-CPT paradigm, participants respond to an ‘X’ probe differently based on whether it was immediately preceded by an ‘A’ cue or a different cue. However, as it has typically been used in the neuroimaging literature, the AX-CPT paradigm requires selecting between responses and not explicitly withholding from responding in certain contexts. In the present study, we focus on situations in which an individual can prepare in advance to refrain from responding to a particular stimulus based on contextual information, and how the activation of the corresponding goal state changes how this response-irrelevant stimulus is processed.

The process of deciding how to respond requires the ability to ignore irrelevant information and maintain focus on the stimuli and rules that dictate the correct course of action. A network of brain regions referred to as the default mode network (DMN), which includes the posterior cingulate cortex (PCC), medial PFC, and ventral precuneus, often appears to be suppressed during the performance of a variety of tasks involving cognitive control (Shulman et al., 1997). As activation within task-positive brain networks increases, activation within the DMN typically decreases, suggesting a competitive relationship between the processing of external stimulus information and the DMN (e.g., Greicius et al., 2003, Uddin et al., 2009). Importantly, the DMN has been strongly linked to information processing in the absence of a task (e.g., Raichle et al., 2001, Shulman et al., 1997), the activation of which is often hypothesized to reflect internal thought (e.g., Sheline et al., 2009). More recent evidence suggests the activity within the DMN has consequences for goal-directed behavior. Greater activation within this network is associated with mind wandering (Weissman, Roberts, Visscher, & Woldorff, 2006), “zoning out,” and diminished performance during a demanding task (Esterman, Noonan, Rosenberg, & DeGutis, 2013).

Such prior demonstrations suggest that activation within the DMN is detrimental to the execution of cognitive control processes, interfering with the ability to carry out goal-directed behavior. Under certain conditions, however, it might be advantageous to disengage from task-related information processing, particularly when the desired outcome is to avoid responding. We hypothesized that when the task involves the need to refrain from responding contingent on a flexibly configured goal state, activation within the DMN might serve to support contextually-appropriate non-responding. Here, we examine the neural correlates of processing a response-irrelevant stimulus.

We recently developed a paradigm for investigating flexible, goal-contingent response inhibition (Anderson & Folk, 2014; see also 2012a). Participants report the identity of a centrally-presented target letter only if its color matches that of a cue at the beginning of each trial. Immediately preceding the target, irrelevant flanker letters are presented. These flankers can be either compatible or incompatible with the target-associated response, and can be rendered in either the cued (response-relevant) or the uncued (response-irrelevant) color. Despite the fact that the flankers never require a response and are thus task-irrelevant, the processing of these flankers is strongly modulated by whether their color is response-relevant. When the flankers are rendered in the response-relevant color, they elicit a compatibility effect indicative of the activation of their associated response, whereas when they are rendered in the response-irrelevant color, they elicit a robust reverse compatibility effect indicative of the inhibition of their associated response.

In the present study, we investigated the brain systems underlying the processing of response-irrelevant compared to response-relevant stimuli. By including flanker-only trials during which the target was omitted, we isolated the modulatory impact of current goals on stimulus processing from overt action/inaction (see Serences et al., 2005, for a similar design concept in the context of contingent attentional capture). Our findings reveal a role for the DMN in goal-contingent response inhibition, thereby actively supporting human cognitive control.