fMRI reveals reciprocal inhibition between social and physical cognitive domains

The first hypothesis is directly related to the “task-positive” and “task negative” (or “default mode”) labels, which have come to be associated with the two networks (Raichle et al., 2001). These labels were suggested by early findings that a broad range of tasks activate the TPN and deactivate the DMN (Shulman et al., 1997). This hypothesis predicts that it should not be possible to identify goal-directed tasks that activate the DMN and/or deactivate the TPN. It is challenged by more recent findings that identify goal-directed tasks which activate the DMN above a resting baseline (Iacoboni, 2004, Sestieri et al., 2010, Spreng et al., 2010), including one task which demonstrates parametric increases in DMN activity associated with social working memory load (Meyer et al., 2012). Hence Spreng (2012) suggests that the labels ‘task positive’ and ‘task negative’ are “more likely the byproduct of the desire for rigorously controlled experimental designs (i.e., externally directed stimuli) than meaningful descriptors of functional brain networks.”

The second hypothesis appeals to attention to account for the tension between the TPN and DMN (Broyd et al., 2009, Buckner and Carroll, 2007, Buckner et al., 2008). These accounts build on the observation that a common feature of tasks that activate the TPN and deactivate the DMN is focused attention to the external environment. According to various accounts, focused attention may be in competition either with broad exploratory attention (Gilbert et al., 2007), or with a variety of types of internal attention, including attention to self (Andrews-Hanna, 2012, Fransson, 2006, Gusnard, 2001), conceptual association (Bar, 2009, Binder et al., 1999), episodic retrieval (Buckner and Carroll, 2007), and mental simulation or model building (Spreng et al., 2010). One study has presented evidence for both activation of DMN regions and deactivation of TPN regions (Spreng et al., 2010). On this basis, the authors argue for a variant of the internal versus external attention account. The TPN comprises regions which lie in two distinct networks, as defined by positive functional connectivity: the dorsal attention network (DAN) and the fronto-parietal control network (FPCN). Spreng (2012) argues the TPN does not represent a unitary functional network, but rather reflects distinct cognitive factors which are confounded in many tasks. Hence, Spreng argues that the tension between the TPN and the DMN is a ‘false dichotomy.’ Instead, Spreng suggests that the true tension lies between the DAN and the DMN, and reflects “competition between exogenous and endogenous loci of information processing.” However, this account runs into three difficulties. First, findings from resting state functional connectivity indicate that the regions which are most anti-correlated with the DMN lie in both the FPCN and the DAN.² Since these analyses are neutral with regard to task, the value of characterizing the TPN as a network in tension with the DMN cannot be explained away by appeal to task confounds. Second, there have not been any demonstrations of goal-directed tasks which activate the DMN while deactivating the entire TPN. Spreng et al. (2010) show deactivation of the DAN alongside activation of both the DMN and FPCN. However, that study does not identify specific deactivated regions, and therefore does not demonstrate alignment between task induced activations/deactivations and anti-correlated regions derived from functional connectivity. Third, the cognitive characterization of the tension as being due to internal versus external attention appears problematic for one class of tasks which have been consistently associated with the DMN. A large number of studies have implicated the DMN in social cognition (Amodio and Frith, 2006, Mars et al., 2012, Schilbach et al., 2008, Van Overwalle, 2009). Many of these tasks differ from other tasks which are classified as involving internally directed cognition in a significant respect: they require attention to external stimuli. For instance, (Iacoboni, 2004) finds activation of the default network above resting levels while participants watch videos of unfamiliar individuals engaged in social interactions. Social cognition tasks may essentially involve attention to ‘internal states’, however, these are often the ‘internal states’ of unfamiliar individuals, not of the participant.

The third hypothesis, which we favor, is the ‘opposing domains hypothesis’. According to this hypothesis, the task positive and task negative networks reflect two incompatible cognitive modes, each of which can be directed towards understanding the external world. Instead of appealing to attention, this hypothesis is more closely allied to dual-process models of cognition, which hold that distinct cognitive modes can be engaged by externally directed tasks (Evans, 2003, Kahneman, 2003, Sloman, 1996). These modes are hypothesized to be associated with two broad cognitive domains, namely social information processing (reasoning about the minds of others) and non-social information processing (reasoning about physical objects). The opposing domains hypothesis is motivated by theoretical work in a distinct literature on the problem of consciousness (Hill, 1997, Jack and Shallice, 2001, Levine, 2000, Nagel, 1974, Robbins and Jack, 2006), however for current purposes we focus on considering this hypothesis as a candidate for explaining the tension between the TPN and DMN. A direct prediction of both this hypothesis and the internal vs. external attention hypothesis is that, in addition to tasks that activate the task positive network and deactivate the task negative network, it should also be possible to identify goal-directed tasks that activate the task negative network and deactivate the task positive network. In other words, it should be possible to identify goal directed tasks that push the see-saw to both extremes of its full range of motion. Further, since the definition of the TPN and DMN was initially established by reference to anti-correlated networks seen in resting connectivity (Fox et al., 2005), there should be a close correspondence between these anti-correlated networks and the regions shown to be in tension by the tasks. The key difference between these hypotheses is that the internal vs. external attention hypothesis predicts this pattern should be produced by external and internal tasks, even when the social processing demands of the tasks are similar. In contrast, the opposing domains hypothesis predicts that this pattern should be produced by social and non-social tasks, even when the attention demands of the tasks are similar. We know of no reports which test the first prediction, as existing reports confound internal focus with social processing (Sestieri et al., 2010, Spreng et al., 2010). The present study aims to test the second prediction.