A framework for understanding the relationship between externally and internally directed cognition Matthew L. Dixon a,n , Kieran C.R. Fox a , Kalina Christoff a,b,nn a Department of Psychology, University of British Columbia, 2136 West Mall, Vancouver, BC, Canada V6T 1Z4 b Brain Research Centre, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 article info Keywords: Externally directed cognition Internally directed cognition Lateral prefrontal cortex Default mode network Cognitive control Mind wandering Self-referential Medial prefrontal cortex abstract Externally directed cognition (EDC) involves attending to stimuli in the external environment, whereas internally directed cognition (IDC) involves attending internally to thoughts, memories and mental imagery. To date, most studies have focused on the competition or trade-offs between these modes of cognition. However, both EDC and IDC include a variety of cognitive states that differ along multiple dimensions. These dimensions may influence the way in which EDC and IDC relate to each other. In this review, we present a novel framework that considers whether cognitive resources are oriented externally or internally, and also whether a given cognitive state involves intentional (i.e., voluntary) or spontaneous (i.e., involuntary) processing. Within this framework, we examine the conditions under which EDC and IDC are expected to either compete, or co-occur without interference. We argue that EDC and IDC are not inherently antagonistic, but when both involve higher levels of intentionality they are increasingly likely to compete, due to the capacity limitations of intentional processing. In contrast, if one or both involve spontaneous processing, EDC and IDC can co-occur with minimal interference given that involuntary processes are not subject to the same capacity constraints. A review of the brain regions implicated in EDC and IDC suggests that their neural substrates are partially segregated and partially convergent. Both EDC and IDC recruit the lateral prefrontal cortex (PFC) during intentional processing, and may therefore compete over the processes and representational space it supports. However, at lower levels of intentionality, EDC and IDC rely on largely distinct neural structures, which may enable their co-occurrence without interference. The proposal that EDC and IDC can in some cases co-occur, provides a framework for understanding the complex mental states that underlie theory of mind, creativity, the influence of self-evaluative processing on cognitive control, and memory-guided attention. & 2014 Elsevier Ltd. All rights reserved. 1. Introduction At one moment, our attention could be directed externally to a conversation with a friend, and at the next moment, it could be directed internally to plans for the coming evening. This common situation illustrates a key distinction between externally and internally directed cognition (EDC and IDC, respectively). Cognitive neuroscience research has traditionally focused on EDC, utilizing selective attention, cognitive control, and other tasks that involve processing and responding to externally presented stimuli. More recently, however, IDC has gained more widespread appreciation with the discovery of the default mode network (DMN). The DMN is a collection of regions that are suppressed during a variety of tasks that demand external attention (Shulman et al., 1997), and are activated during the ‘resting state’ (Gusnard & Raichle, 2001), which is ostensibly dominated by internally directed self-referential cognitive processes (Buckner, Andrews-Hanna, & Schacter, 2008). IDC has also garnered interest with the growing scientific investigation of mind wandering — a prevalent form of cognition characterized by an internal train of thought that is often unrelated to the immediate sensory environment, and that usually competes with externally directed task performance (Christoff, 2012; Christoff, Gordon, Smallwood, Smith, & Schooler, 2009; Kam & Handy, 2013; Kane & McVay, 2012; Killingsworth & Gilbert, 2010; Mason et al., 2007; Schooler et al., 2011). At first glance, EDC and IDC may appear to be mutually exclusive modes of cognition vying for the same cognitive resources, and it is often assumed that when one of these modes is operating, the other is automatically suppressed. This perspective is based on empirical work which has demonstrated that: (1) periods of mind wandering are associated with errors in externally directed task performance Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/neuropsychologia Neuropsychologia http://dx.doi.org/10.1016/j.neuropsychologia.2014.05.024 0028-3932/& 2014 Elsevier Ltd. All rights reserved. n Corresponding author. Tel.: þ1 604 822 2849; fax: þ1 604 822 6923. nn Corresponding author at: Department of Psychology, University of British Columbia, 2136 West Mall, Vancouver, BC,Canada V6T 1Z4. Tel.: þ1 604 822 4610; fax: þ1 604 822 6923. E-mail addresses: mattdixon@psych.ubc.ca (M.L. Dixon), kchristoff@psych.ubc.ca (K. Christoff). Please cite this article as: Dixon, M. L., et al. A framework for understanding the relationship between externally and internally directed cognition. Neuropsychologia (2014), http://dx.doi.org/10.1016/j.neuropsychologia.2014.05.024i Neuropsychologia ∎ (∎∎∎∎) ∎∎∎–∎∎∎