Abstract

Discourse comprehension is a hallmark of human social behaviour and refers to the act of interpreting a written or spoken message by constructing mental representations that integrate incoming language with prior knowledge and experience. Here, we report a human lesion study (n = 145) that investigates the neural mechanisms underlying discourse comprehension (measured by the Discourse Comprehension Test) and systematically examine its relation to a broad range of psychological factors, including psychometric intelligence (measured by the Wechsler Adult Intelligence Scale), emotional intelligence (measured by the Mayer, Salovey, Caruso Emotional Intelligence Test), and personality traits (measured by the Neuroticism-Extraversion-Openness Personality Inventory). Scores obtained from these factors were submitted to voxel-based lesion-symptom mapping to elucidate their neural substrates. Stepwise regression analyses revealed that working memory and extraversion reliably predict individual differences in discourse comprehension: higher working memory scores and lower extraversion levels predict better discourse comprehension performance. Lesion mapping results indicated that these convergent variables depend on a shared network of frontal and parietal regions, including white matter association tracts that bind these areas into a coordinated system. The observed findings motivate an integrative framework for understanding the neural foundations of discourse comprehension, suggesting that core elements of discourse processing emerge from a distributed network of brain regions that support specific competencies for executive and social function.

Introduction

Discourse comprehension is the act of interpreting a written or spoken message by constructing mental representations that integrate incoming language with prior knowledge and experience. To illustrate, consider the proposition, ‘Michelle ordered a drink at the bar’. The meaning of the verb ‘ordered’ entails that she carried out a series of actions that resulted in a drink being delivered. The fact that we tend to interpret the sentence as ordering an alcoholic drink illustrates the role of background knowledge. Thus, discourse comprehension depends on understanding syntactic expressions (e.g. the meaning of the verb ‘to order’) that additionally incorporate background knowledge and experience to support a coherent understanding of the discourse as a whole (e.g. that Michelle is likely to order a specific type of drink and to be at a particular location, on a specific occasion, with specific people, etc.).

According to an influential theory of discourse processing (Dijk and Kintsch, 1983; Zwaan and Radvansky, 1998), understanding discourse depends on a mental model of what the written or spoken message says (the text base), in addition to a mental representation of what the message is about (the situation model). The propositional structure of the message is represented by the written or spoken sentence(s) and is supplemented by inferences that make the meaning of the sentence(s) locally coherent (e.g. by integrating multiple propositional elements of a complex message). The situation model is formed from the text base by combining background knowledge and experience to support a specific spatial, temporal, and/or psychological vantage point from which we perceive and understand the event(s). According to this framework, mental representations of the text base primarily depend on language processes that capture the propositional structure of the written or spoken message. In contrast, a situation model depends on executive functions for the integration of non-propositional and non-verbal information that represents the spatial, temporal, and/or psychological context for understanding the event(s). Contemporary research and theory on discourse comprehension investigates the nature of these representations, their neurobiological foundations, and how these representations unfold during online comprehension to support goal-directed social behaviour (Stemmer and Whitaker, 2008).

Neuroscience evidence indicates that a distributed network of cortical regions supports mental representations of word-level processes for understanding what a written or spoken message says (the text base). This network entails classic perisylvian language areas within the middle and superior temporal gyri and inferior frontal cortex (Robertson et al., 1988; Huettner et al., 1989; Binder et al., 1994; Fletcher et al., 1995; Fiez and Petersen, 1998; Maguire et al., 1999; St George et al., 1999; Giraud et al., 2000; Ferstl and von Cramon, 2001, 2002; Vogeley et al., 2001; Turkeltaub et al., 2002; Ferstl et al., 2005; Xu et al., 2005; Vigneau et al., 2006; Hasson et al., 2007). Recent neuroscience evidence further indicates that specific cortical regions are preferentially engaged during the comprehension of coherent and connected texts, beyond comprehension of word-level representations. The observed cortical regions include the anterior temporal lobes (Stowe et al., 1998; Ferstl et al., 2008) and orbitofrontal cortex (Xu et al., 2005; Hasson et al., 2007; Egidi and Caramazza, 2013), which are each high-level association cortices that integrate information across multiple brain systems and are believed to play an important role in the neural representation of situation models.

Accumulating neuroscience evidence further indicates that inferential processes for building coherent mental models that integrate incoming language with prior knowledge and experience depend on a distributed network of frontal and parietal brain regions (Badre and Wagner, 2006; Glascher et al., 2010; Barbey et al., 2012b). The fronto-parietal network includes lateral frontopolar cortex, anterior prefrontal cortex, dorsolateral prefrontal cortex, anterior cingulate/medial prefrontal cortex, and the inferior and superior parietal lobe. This constellation of regions is commonly engaged by tasks that require executive control processes (Ramnani and Owen, 2004). The fronto-parietal network is recruited by paradigms that elicit controlled processing related to the simultaneous consideration of multiple interdependent contingencies (Kroger et al., 2002), conflicting stimulus-response mappings (Crone et al., 2006), and integrating working memory with attentional resource allocation (Koechlin et al., 1999). In addition, many of the regions in the fronto-parietal network show sustained activity over the duration of a task block (Dosenbach et al., 2006), supporting the maintenance and integration of items for goal-directed behaviour. Thus, emerging evidence indicates that discourse comprehension may depend on a fronto-parietal network that supports the integration and control of cognitive representations and provides a neural architecture for building coherent mental models that integrate incoming language with prior knowledge and experience (Botvinick et al., 2001; Miller and Cohen, 2001; Duncan, 2010).

The neuroscience literature on discourse comprehension is characterized by additional questions that remain the focus of ongoing research and scientific exchange. First, the degree to which discourse comprehension preferentially engages brain mechanisms within the left versus right hemisphere remains unclear. For example, investigators have proposed that general cognitive mechanisms for attention, memory, and executive processes within the left hemisphere are critical for discourse comprehension (Maguire et al., 1999). Alternatively, research suggests that a core facet of discourse comprehension is the interpretation of non-literal meanings and that discourse comprehension may therefore engage a right lateralized brain network that supports inductive inference (Winner et al., 1998; Brownell and Stringfellow, 1999; Beeman et al., 2000; Robertson et al., 2000). Second, it is unclear whether discourse comprehension depends on narrative-specific neural systems or a broader set of neural mechanisms for social information processing (Glascher et al., 2010; Barbey et al., 2012b; Barbey et al., 2012a). A network of neural correlates has been linked to social and emotional processing using a range of experimental materials such as interpersonal scenarios, cartoons, jokes, sarcasm, faux pas, and moral and ethical dilemmas (Adolphs, 2010). Analysis of the specialized contributions of regions within the social knowledge network has suggested, for example, that the orbitofrontal cortex plays a key role in the representation of mental states, both for an individual’s own thoughts and beliefs and those of others, and the left anterior temporal lobe is involved in storing relevant social knowledge, which contributes to the contextual understanding of others’ social interactions (Frith and Frith, 2003; Sabbagh, 2004; Saxe, 2006). Thus, the observed network engages regions implicated in discourse comprehension and may reflect key competencies for social information processing. In addition, research on discourse comprehension in cognitive ageing indicates that decline in semantic integration in comprehension of written texts is associated with recall abilities (measured by reading span) and emotional regulation (Maguire et al., 1999; Smiler et al., 2003; Egidi and Nusbaum, 2012; Payne et al., 2012), further suggesting a dependency between discourse comprehension and executive, social and emotional processes. Finally, the contribution of mechanisms for learning and memory to discourse comprehension remains to be well characterized. Behaviourally, the use of situation models aids comprehension and memory of discourse considerably (Gernsbacher, 1990) and an emerging body of neuroscience evidence further suggests that discourse comprehension and production abilities may critically depend on executive and attentional processes within the prefrontal cortex (Alexander, 2006; Ferstl et al., 2008).

Research on the neural bases of discourse comprehension would therefore benefit from a more precise characterization of its cognitive foundations, applying a psychometric approach to identify key competencies of discourse comprehension and their relation to a broad spectrum of psychological factors. The application of lesion methods to map the information processing architecture of discourse comprehension would further advance our understanding of the mechanisms that give rise to discourse processing (Glascher et al., 2010; Woolgar et al., 2010; Barbey et al., 2012b). Neuropsychological patients with focal brain lesions provide a valuable opportunity to study the neural mechanisms of discourse processing, supporting the investigation of lesion-deficit associations that elucidate the role(s) of specific brain structures. Accumulating evidence suggests, for example, that social-communicative deficits after brain injury may result from damage to the prefrontal cortex and deficits in the ability to represent situation models that guide the selection and control of responses to social stimuli (Barbey et al., 2009a; Barbey et al., 2009b; Adolphs, 2010; Barbey, 2011a; Barbey et al., 2013a, in press). Although the neural foundations of discourse processing remain to be assessed using lesion mapping methods, the broader neuropsychological patient literature has provided significant insight into the neural bases of higher cognitive functions, such as general intelligence (Basso et al., 1973; Black, 1976; Eslinger and Damasio, 1985; Shallice and Burgess, 1991; Bechara et al., 1994; Duncan et al., 1995; Burgess and Shallice, 1996; Isingrini and Vazou, 1997; Parkin and Java, 1999; Blair and Cipolotti, 2000; Kane and Engle, 2002; Bugg et al., 2006; Glascher et al., 2009, 2010; Roca et al., 2010; Barbey et al., 2012b) and working memory (D’Esposito and Postle, 1999; Muller et al., 2002; Baldo and Dronkers, 2006; D’Esposito et al., 2006; Volle et al., 2008; Tsuchida and Fellows, 2009). These studies, however, share one or more of the following features: diffuse (rather than focal) brain lesions, lack of comparison subjects carefully matched for pre- and post-injury performance measures, exclusive use of cognitive tests without an assessment of discourse comprehension, and lack of latent variable modelling to derive error-free indices of the psychological constructs of interest. As a consequence, there has been no comprehensive evaluation of discourse comprehension in a relatively large sample of patients with focal brain damage, and across a broad range of tasks and stimulus material.

Motivated by these considerations, the cognitive and neural bases of discourse comprehension were studied here in a large sample of patients with focal brain injuries (n = 145). Discourse comprehension was analysed in relation to a broad set of psychological factors, including psychometric intelligence (Wechsler Adult Intelligence Scale), emotional intelligence (Mayer, Salovey, Caruso Emotional Intelligence Test), and personality traits (Neuroticism-Extroversion-Openness Personality Inventory). Finally, voxel-based lesion-symptom mapping was applied to elucidate the underlying information processing architecture, identifying core brain mechanisms that support discourse comprehension.

Materials and methods

Participant data

Participants were drawn from the Phase 3 Vietnam Head Injury Study (VHIS) registry, which includes American male veterans who suffered brain damage from penetrating head injuries in the Vietnam War (n = 145). All subjects gave informed written consent. Phase 3 testing occurred between April 2003 and November 2006. Demographic and background data for the VHIS are reported in Supplementary Table 1 (Koenigs et al., 2009; Raymont et al., 2010; Barbey et al., 2011b, 2012b). No effects on test performance were observed in the VHIS sample on the basis of demographic variables (e.g. age, years of education, lesion size).

Lesion analysis

CT data were acquired during the Phase 3 testing period. Axial CT scans without contrast were acquired at Bethesda Naval Hospital on a GE Medical Systems Light Speed Plus CT scanner in helical mode (150 slices per subject, field of view covering head only). Images were reconstructed with an in-plane voxel size of 0.4 × 0.4 mm, overlapping slice thickness of 2.5 mm, and a 1 mm slice interval. Lesion location and volume were determined from CT images using the Analysis of Brain Lesion software (Makale et al., 2002; Solomon et al., 2007) contained in MEDx v3.44 (Medical Numerics) with enhancements to support the Automated Anatomical Labeling atlas (Tzourio-Mazoyer et al., 2002). Lesion volume was calculated by manual tracing of the lesion in all relevant slices of the CT image then summing the traced areas and multiplying by slice thickness. Lesion tracing included grey and white matter regions damaged as a consequence of penetrating head injury (e.g. incorporating coup–contrecoup effects and axonal injury). We note that the effects of penetrating head injuries are more focal and less susceptible to diffuse axonal injury than typical blunt head injuries. A trained neurologist performed the manual tracing, which was then reviewed by an observer who was blind to the results of the neuropsychological testing. As part of this process, the CT image of each subject’s brain was spatially normalized to a CT template brain image. This template was created by spatial normalization of a neurologically healthy individual’s CT brain scan to MNI space (Collins et al., 1994) using the Automated Image Registration program (Woods et al., 1993). For each subject, a lesion mask image in MNI space was saved for voxel-based lesion-symptom mapping (Bates et al., 2003). This method applies a Mann-Whitney U-test to compare, for each voxel, scores from patients with a lesion at that voxel contrasted against those without a lesion at that voxel. The reported findings were thresholded using a False Discovery Rate correction of q < 0.01. To ensure sufficient statistical power for detecting a lesion-deficit correlation, our analysis only included voxels for which three or more patients had a lesion. The lesion overlap map for the entire VHIS patient sample is illustrated in Supplementary Fig. 1.

Psychological measures

We administered the Discourse Comprehension Test, which is designed to provide information about language comprehension as it occurs in natural communicative interactions (Brookshire and Nicholas, 1984; Wegner et al., 1984; Nicholas and Brookshire, 1986). The Discourse Comprehension Test assesses comprehension and retention of stated and implied main ideas and details from 10 stories with questions that require yes/no responses. ‘Main ideas’ represent what is most relevant or important (i.e. the gist) and provide an overall unity to discourse. In contrast, ‘details’ represent specific elements of discourse that may be peripheral to the main ideas. Whereas main ideas are expressed by phrases or sentences, details are typically encoded by individual elements of discourse (e.g. nouns, verbs, etc.). Finally, the directness of main ideas and details may be stated ‘explicitly’ or ‘implied’ in the text. The stories of the Discourse Comprehension Test are controlled for length, grammatical complexity, listening difficulty and information content. In addition, we administered the Wechsler adult intelligence scale, third edition (WAIS-III; Wechsler, 1997), the Mayer, Salovey, Caruso Emotional Intelligence Test (MSCEIT; Mayer et al., 2008), and the Neuroticism-Extraversion-Openness Personality Inventory (NEO-PI; Costa and McCrae, 2000).

We obtained latent variables representative of psychometric and emotional intelligence as reported by Barbey et al. (2012b). Latent factors for psychometric intelligence were derived from the WAIS-III, namely, verbal comprehension/crystallized intelligence (vocabulary, similarities, information, and comprehension), perceptual organization/fluid intelligence (block design, matrix reasoning, picture completion, picture arrangement, and object assembly), working memory capacity (arithmetic, digit span, and letter-number sequencing), and processing speed (digit symbol coding and symbol search). The MSCEIT allowed the extraction of a general emotional intelligence index (faces, pictures, sensations, facilitation, blends, changes, emotional, and social subtests). Personality traits were measured by the NEO-PI, but treated separately from the cognitive measures. Discourse comprehension scores were obtained directly from the Discourse Comprehension Test (stated/implied main ideas, stated/implied details). Supplementary Table 2 summarizes the employed measures of psychometric and emotional intelligence (for further detail concerning their standardization, reliability, and validity, see Wechsler, 1997; Mayer et al., 2008). Supplementary Table 3 provides descriptive statistics for each of the administered neuropsychological tests.

Voxel-based lesion-symptom mapping

The obtained scores were correlated to regional grey and white matter determined by voxel-based lesion-symptom mapping (Bates et al., 2003). This method compares, for every voxel, scores from patients with a lesion at that voxel contrasted against those without a lesion at that voxel. This approach can help to identify brain regions that are important for the constructs of interest by mapping where damage can interfere with performance (Glascher et al., 2010; Woolgar et al., 2010; Barbey et al., 2012b; Barbey et al., 2012a; Barbey et al., in press).

Results

Behavioural results

Table 1 reports the correlation matrix for the 12 measures of interest. Note that discourse comprehension performance showed significant correlations with all the psychometric and emotional intelligence scores (from r = 0.28 to r = 0.36). Extraversion was the personality trait more highly correlated with discourse comprehension (r = −0.15). These are moderate correlations, meaning that there is substantial variance left in discourse comprehension performance. Therefore, we computed stepwise regression analyses for obtaining residual discourse comprehension scores orthogonal to its significant predictors, as explained below.

Table 1

Correlation matrix for all scores (n = 145), P-values are shown

 10 11 12 
1. Latent WAIS Verbal Comprehension  0.585 0.755 0.446 0.809 −0.071 0.107 −0.007 −0.083 0.308 0.322 0.039 
  0.000 0.000 0.000 0.000 0.398 0.200 0.933 0.320 0.000 0.000 0.644 
2. Latent WAIS Perceptual Organization   0.646 0.794 0.550 −0.042 0.147 0.005 −0.069 0.177 0.283 0.070 
   0.000 0.000 0.000 0.615 0.079 0.951 0.413 0.033 0.001 0.405 
3. Latent WAIS Working Memory    0.602 0.607 0.035 0.114 −0.023 −0.128 0.186 0.364 0.076 
    0.000 0.000 0.676 0.172 0.786 0.125 0.025 0.000 0.365 
4. Latent WAIS Processing Speed     0.498 0.039 −0.001 0.020 −0.070 0.097 0.284 0.089 
     0.000 0.642 0.993 0.812 0.403 0.245 0.001 0.288 
5. Latent Emotional Intelligence      −0.060 0.133 0.193 −0.078 0.273 0.333 0.041 
      0.476 0.110 0.020 0.352 0.001 0.000 0.624 
6. NEO: Extraversion       0.129 −0.001 −0.246 0.163 −0.148 −0.156 
       0.122 0.994 0.003 0.050 0.075 0.062 
7. NEO: Agreeableness        −0.068 −0.239 0.122 0.079 0.037 
        0.419 0.004 0.142 0.343 0.660 
8. NEO: Conscientiousness         0.059 0.018 0.002 −0.031 
         0.480 0.831 0.977 0.709 
9. NEO: Neuroticism          −0.064 −0.136 −0.106 
          0.442 0.103 −0.106 
10. NEO: Openness           0.016 −0.074 
           0.847 0.378 
11. Discourse Comprehension: Overall Score            0.945 
            0.000 
12. Discourse Comprehension Residual             
 10 11 12 
1. Latent WAIS Verbal Comprehension  0.585 0.755 0.446 0.809 −0.071 0.107 −0.007 −0.083 0.308 0.322 0.039 
  0.000 0.000 0.000 0.000 0.398 0.200 0.933 0.320 0.000 0.000 0.644 
2. Latent WAIS Perceptual Organization   0.646 0.794 0.550 −0.042 0.147 0.005 −0.069 0.177 0.283 0.070 
   0.000 0.000 0.000 0.615 0.079 0.951 0.413 0.033 0.001 0.405 
3. Latent WAIS Working Memory    0.602 0.607 0.035 0.114 −0.023 −0.128 0.186 0.364 0.076 
    0.000 0.000 0.676 0.172 0.786 0.125 0.025 0.000 0.365 
4. Latent WAIS Processing Speed     0.498 0.039 −0.001 0.020 −0.070 0.097 0.284 0.089 
     0.000 0.642 0.993 0.812 0.403 0.245 0.001 0.288 
5. Latent Emotional Intelligence      −0.060 0.133 0.193 −0.078 0.273 0.333 0.041 
      0.476 0.110 0.020 0.352 0.001 0.000 0.624 
6. NEO: Extraversion       0.129 −0.001 −0.246 0.163 −0.148 −0.156 
       0.122 0.994 0.003 0.050 0.075 0.062 
7. NEO: Agreeableness        −0.068 −0.239 0.122 0.079 0.037 
        0.419 0.004 0.142 0.343 0.660 
8. NEO: Conscientiousness         0.059 0.018 0.002 −0.031 
         0.480 0.831 0.977 0.709 
9. NEO: Neuroticism          −0.064 −0.136 −0.106 
          0.442 0.103 −0.106 
10. NEO: Openness           0.016 −0.074 
           0.847 0.378 
11. Discourse Comprehension: Overall Score            0.945 
            0.000 
12. Discourse Comprehension Residual             

NEO = Neuroticism-Extraversion-Openness.

Stepwise regression

Psychometric intelligence factors (verbal comprehension, fluid intelligence, working memory, and processing speed) and emotional intelligence, along with personality traits were submitted to a stepwise regression analysis; discourse comprehension was the dependent measure. The results showed that working memory and extraversion reliably predict discourse comprehension. Standardized beta values were: working memory (β = 0.37, P = 0.000) and extraversion (β = −0.16, P = 0.04). Therefore, higher working memory scores and lower extraversion scores predict better discourse comprehension performance. The variance unexplained by working memory and extraversion defined a residual discourse comprehension score that was also submitted to lesion analysis.

Discourse comprehension: lesion results

Discourse comprehension was associated with a distributed network of brain regions within the left and right hemisphere (Fig. 1). Significant effects encompassed locations for: (i) language processing (e.g. Broca’s area and superior temporal gyrus); (ii) spatial processing (e.g. inferior and superior parietal cortex); (iii) motor processing (e.g. somatosensory and primary motor cortex); and (iv) working memory (e.g. dorsolateral prefrontal cortex, inferior and superior parietal cortex, and superior temporal gyrus); in addition to expected locations of major white matter fibre tracts, including (v) the anterior and dorsal bundle of the superior longitudinal/arcuate fasciculus connecting temporal, parietal, and inferior frontal regions; (vi) the superior fronto-occipital fasciculus connecting dorsolateral prefrontal cortex and the frontal pole with the superior parietal lobule; and (vii) the uncinate fasciculus, which connects anterior temporal cortex and amygdala with orbitofrontal and frontopolar regions. This pattern of findings suggests that discourse comprehension reflects the ability to integrate verbal, spatial, motor, and executive processes through a circumscribed set of cortical connections within the left and right hemisphere.

Figure 1

Voxel-based lesion-symptom mapping of discourse comprehension (n = 145). The illustrated results are thresholded at q < 0.01 (using a false discovery rate correction for multiple comparisons). In each axial slice, the right hemisphere is to the left.

Figure 1

Voxel-based lesion-symptom mapping of discourse comprehension (n = 145). The illustrated results are thresholded at q < 0.01 (using a false discovery rate correction for multiple comparisons). In each axial slice, the right hemisphere is to the left.

Working memory: lesion results

As illustrated in Fig. 2, discourse comprehension shared neural substrates with working memory, engaging left inferior [Brodmann area (BA) 7] and superior parietal regions (BA 40), and right dorsolateral prefrontal cortex (BA 9) (Fig. 2). These frontal and parietal regions have been widely implicated in the maintenance, monitoring and manipulation of representations in working memory (Wager and Smith, 2003; Owen et al., 2005) and provide evidence in this context for their central roles in discourse comprehension.

Figure 2

Voxel-based lesion-symptom mapping of working memory (n = 145). The illustrated results are thresholded at q < 0.01 (using a false discovery rate correction for multiple comparisons). In each axial slice, the right hemisphere is to the left.

Figure 2

Voxel-based lesion-symptom mapping of working memory (n = 145). The illustrated results are thresholded at q < 0.01 (using a false discovery rate correction for multiple comparisons). In each axial slice, the right hemisphere is to the left.

Residual discourse comprehension scores: lesion results

We analysed the discourse comprehension residual scores removing variance shared with its significant predictors. As Table 1 illustrates, the discourse comprehension residual scores were not reliably correlated with any of the psychometric, emotional, or personality variables examined in the present study (e.g. verbal comprehension, perceptual organization, working memory, etc.). This residual factor captures the unique variance associated with discourse comprehension and supports an assessment of the core brain mechanisms underlying discourse processes. Similar findings for the discourse comprehension latent and residual scores are expected due to the large correlation between these factors (r = 0.94, P = 0.000). Impairment in the discourse comprehension residual score was associated with selective damage to frontal and parietal brain structures that have been widely implicated in executive (Miller and Cohen, 2001) and social function (Ochsner and Lieberman, 2001; Ochsner, 2004). These regions comprised bilateral orbitofrontal cortex (BA 10), bilateral inferior (BA 40) and superior parietal cortex (BA 7), in addition to major white matter fibre tracts, including the superior longitudinal/arcuate fasciculus and the superior fronto-occipital fasciculus (Fig. 3). The observed pattern of findings indicates that discourse comprehension is centrally supported by executive, social, and emotional processes (Ochsner and Lieberman, 2001; Ochsner, 2004).

Figure 3

Voxel-based lesion-symptom mapping of discourse comprehension and discourse comprehension (residual) (n = 145). Lesion overlap map illustrating common and distinctive brain regions for discourse comprehension (blue) and discourse comprehension residual (yellow) (n = 145; q < 0.01). Overlap between these factors is illustrated in green. In each axial slice, the right hemisphere is to the left.

Figure 3

Voxel-based lesion-symptom mapping of discourse comprehension and discourse comprehension (residual) (n = 145). Lesion overlap map illustrating common and distinctive brain regions for discourse comprehension (blue) and discourse comprehension residual (yellow) (n = 145; q < 0.01). Overlap between these factors is illustrated in green. In each axial slice, the right hemisphere is to the left.

Discussion

We investigated the neural bases of discourse comprehension and systematically examined their contributions to a broad set of psychological factors, including psychometric intelligence, emotional intelligence, and personality traits. Using a relatively large sample of patients with focal brain injuries (n = 145), we report several main findings.

First, raw correlations among psychometric intelligence (verbal comprehension/crystallized intelligence, perceptual organization/fluid intelligence, working memory, and processing speed), emotional intelligence, personality traits, and discourse comprehension showed that (i) psychometric and emotional intelligence scores were positively correlated with discourse comprehension; and (ii) extraversion was negatively correlated with discourse comprehension. Therefore, discourse comprehension depends on psychometric and emotional intelligence factors and the regulation of social information processing (reduction in impulsivity and inappropriate social behaviour associated with high levels of extraversion).

Second, stepwise regression analyses showed that working memory capacity and extraversion reliably predict discourse comprehension performance. This result indicates that verbal comprehension, perceptual organization, processing speed, and emotional intelligence are no longer related to discourse comprehension. The regression analysis also demonstrated that there is a substantial proportion of discourse comprehension variance that is unexplained by the considered predictors.

Third, voxel-based lesion-symptom mapping of discourse comprehension and its reliable predictors revealed that these convergent variables engage a shared network of frontal and parietal regions. The observed findings contribute to the neuropsychological patient evidence indicating that damage to a distributed network of frontal and parietal regions is associated with impaired performance on tests of executive processing (Jung and Haier, 2007; Chiang et al., 2009; Colom et al., 2009; Glascher et al., 2010; Barbey et al., 2012a; Barbey and Patterson, 2011; 2013b) and social function (Barbey et al., 2012a). Barbey et al. (2012a) applied voxel-based lesion-symptom mapping to elucidate the neural substrates of psychometric g, reporting a left lateralized fronto-parietal network that converges with the pattern of findings observed here. The present study contributes to this research programme by elucidating the relationship between key competencies of intelligence and discourse comprehension, providing evidence that these domains recruit a highly overlapping and broadly distributed network of frontal and parietal regions (Figs 1–3). We further investigated the neural basis of discourse comprehension while removing the variance shared with its significant predictors. This analysis revealed selective damage to frontal and parietal brain structures that have been widely implicated in executive processes (Miller and Cohen, 2001) and social function (Ochsner and Lieberman, 2001; Ochsner, 2004) (Fig. 3).

Accumulating evidence indicates that the fronto-parietal network provides a coordinated architecture for the integration and control of cognitive representations (Glascher et al., 2010; Barbey et al., 2012b). Our findings suggest that mechanisms for integration and control are critical for discourse comprehension—supporting the construction of coherent mental models that integrate incoming language with prior knowledge and experience. In particular, the results indicate that discourse comprehension depends on mental representations that integrate verbal, spatial, motor, and executive processes through a circumscribed set of cortical connections within the left and right hemisphere (Fig. 1). This finding supports theories of discourse comprehension that posit general cognitive mechanisms within the left hemisphere (Maguire et al., 1999) and processes for the interpretation of non-literal meanings within the right hemisphere (Winner et al., 1998; Brownell and Stringfellow, 1999; Beeman et al., 2000; Robertson et al., 2000). Taken together, these results support a multifaceted theory of discourse comprehension that incorporates psychological mechanisms for executive function (i.e. integration and control of cognitive representations, and working memory capacity) and normative social behaviour (i.e. negative correlation with impulsivity and inappropriate social behaviour). Rather than operating on the basis of distinct mechanisms, discourse comprehension appears to share cognitive and neural mechanisms with systems for working memory and social information processing (Figs 1–3).

This conclusion complements emerging psychological research that examines discourse comprehension beyond traditionally studied reader and text variables. The focus of recent investigations includes executive functions (Stoltzfus et al., 1993; Kane et al., 1994; Chiappe et al., 2000), such as the readers’ propensity to monitor their understanding (Theide, 2010), and their reliance upon credible and non-credible information sources (Sparks and Rapp, 2011), in addition to social and emotional factors, such as affective influences on comprehension (Komeda, 2009). A growing number of researchers have suggested that theories of discourse comprehension must account for these types of processes, which constitute our naturalistic comprehension experiences (Gerrig, 1993). Indeed, the observed human lesion results suggest that discourse comprehension depends on mechanisms for executive and social function and provide a cognitive neuroscience framework for understanding naturalistic comprehension experiences.

Finally, it is important to emphasize that the abilities measured by tests of psychometric intelligence, emotional intelligence, and personality do not provide a comprehensive assessment of all human psychological traits. There are other aspects, in addition to those measured here, which may contribute to discourse comprehension. For example, investigating how readers interact with and build meaning from multiple related texts remains an important issue (Goldman, 2004). Consider that the Internet affords individuals the opportunity to read multiple, conflicting accounts of current events (Rouet, 2006), or that history students must integrate across multiple texts to understand a historical incident (Wineburg, 2001). Explaining such everyday experiences requires closer examination of multiple texts and their implications for executive control and working memory (Barbey et al., 2013b, 2013c). Another important issue for discourse comprehension research involves investigating how individuals revise their prior beliefs during discourse comprehension, a process called ‘memory updating’, which has been strongly tied to working memory capacity (Colom, 2008; Martinez et al., 2011). Research on memory updating has examined the types of texts, reader variables, and task instructions that make revision more likely. Readers often rely on information mentioned early in a text, even when that information is discounted or contradicted (Johnson, 1994; O’brien, 2010). Memory updating is facilitated by texts that contain causal explanations for why outdated information is no longer valid (Barbey and Patterson, 2011; Patterson, 2012), or by instructions asking readers to track unfolding text events (Rapp, 2005). Additional research is necessary to examine the types of arguments that effectively encourage belief revision, given particular academic settings and styles of reading. Finally, further research is needed to better characterize the specific cognitive processes that contribute to discourse comprehension given, for example, in the present case it is not possible to isolate the contribution of word- or sentence-level mechanisms and to address the role of specific executive control mechanisms (e.g. inhibitory control, for example, measured by the Stroop task; Stoltzfus et al., 1993; Kane et al., 1994; Chiappe et al., 2000; Raz et al., 2011; Diamond, 2013). Understanding the cognitive and neural architecture of discourse comprehension will ultimately require a comprehensive assessment that examines a broader scope of issues. The reported findings contribute to this emerging research programme, demonstrating that discourse comprehension emerges from a distributed network of brain regions that support specific competencies for executive and social function.

Acknowledgements

We are grateful to S. Bonifant, B. Cheon, C. Ngo, A. Greathouse, V. Raymont, K. Reding, and G. Tasick for their invaluable help with the testing of participants and organization of this study.

Funding

This work was supported by funding from the U.S. National Institute of Neurological Disorders and Stroke intramural research program and a project grant from the United States Army Medical Research and Material Command administered by the Henry M. Jackson Foundation (Vietnam Head Injury Study Phase III: a 30-year post-injury follow-up study, grant number DAMD17-01-1-0675). R. Colom was supported by grant PSI2010-20364 from Ministerio de Ciencia e Innovación [Ministry of Science and Innovation, Spain] and CEMU-2012-004 [Universidad Autonoma de Madrid].

Supplementary material

Supplementary material is available at Brain online.

Abbreviation

    Abbreviation
  • WAIS-III

    Wechsler Adult Intelligence Scale, third edition

References

Adolphs
R
Conceptual challenges and directions for social neuroscience
Neuron
 , 
2010
, vol. 
65
 (pg. 
752
-
67
)
Alexander
MP
Impairments of procedures for implementing complex language are due to disruption of frontal attention processes
J Int Neuropsychol Soc
 , 
2006
, vol. 
12
 (pg. 
236
-
47
)
Badre
D
Wagner
AD
Computational and neurobiological mechanisms underlying cognitive flexibility
Proc Natl Acad Sci USA
 , 
2006
, vol. 
103
 (pg. 
7186
-
91
)
Baldo
JV
Dronkers
NF
The role of inferior parietal and inferior frontal cortex in working memory
Neuropsychology
 , 
2006
, vol. 
20
 (pg. 
529
-
38
)
Barbey
AK
Colom
R
Grafman
J
Distributed neural system for emotional intelligence revealed by lesion mapping
Soc Cogn Affect Neurosci
 , 
2012a
 
in press
Barbey
AK
Colom
R
Grafman
J
Dorsolateral prefrontal contributions to human intelligence
Neuropsychologia
 , 
2013a
, vol. 
51
 (pg. 
1361
-
9
)
Barbey
AK
Colom
R
Grafman
J
Architecture of cognitive flexibility revealed by lesion mapping
NeuroImage
  
in press
Barbey
AK
Colom
R
Paul
EJ
Grafman
J
Architecture of fluid intelligence and working memory revealed by lesion mapping
Brain Struct Funct
 , 
2013b
 
in press
Barbey
AK
Colom
R
Solomon
J
Krueger
F
Forbes
C
Grafman
J
An integrative architecture for general intelligence and executive function revealed by lesion mapping
Brain
 , 
2012b
, vol. 
135
 (pg. 
1154
-
64
)
Barbey
AK
Grafman
J
Decety
J
Cacioppo
J
The prefrontal cortex and goal-directed social behavior
The Oxford handbook of social neuroscience
 , 
2011a
New York
Oxford University Press
(pg. 
349
-
59
)
Barbey
AK
Koenigs
M
Grafman
J
Orbitofrontal contributions to human working memory
Cereb Cortex
 , 
2011b
, vol. 
21
 (pg. 
789
-
95
)
Barbey
AK
Koenigs
M
Grafman
J
Dorsolateral prefrontal contributions to human working memory
Cortex
 , 
2013c
, vol. 
49
 (pg. 
1195
-
205
)
Barbey
AK
Krueger
F
Grafman
J
An evolutionarily adaptive neural architecture for social reasoning
Trends Neurosci
 , 
2009a
, vol. 
32
 (pg. 
603
-
10
)
Barbey
AK
Krueger
F
Grafman
J
Structured event complexes in the medial prefrontal cortex support counterfactual representations for future planning
Philos Trans R Soc Lond B Biol Sci
 , 
2009b
, vol. 
364
 (pg. 
1291
-
300
)
Barbey
AK
Patterson
R
Architecture of explanatory inference in the human prefrontal cortex
Front Psychol
 , 
2011
, vol. 
2
 pg. 
162
 
Basso
A
De Renzi
E
Faglioni
P
Scotti
G
Spinnler
H
Neuropsychological evidence for the existence of cerebral areas critical to the performance of intelligence tasks
Brain
 , 
1973
, vol. 
96
 (pg. 
715
-
28
)
Bates
E
Wilson
SM
Saygin
AP
Dick
F
Sereno
MI
Knight
RT
, et al.  . 
Voxel-based lesion-symptom mapping
Nat Neurosci
 , 
2003
, vol. 
6
 (pg. 
448
-
50
)
Bechara
A
Damasio
AR
Damasio
H
Anderson
SW
Insensitivity to future consequences following damage to human prefrontal cortex
Cognition
 , 
1994
, vol. 
50
 (pg. 
7
-
15
)
Beeman
MJ
Bowden
EM
Gernsbacher
MA
Right and left hemisphere cooperation for drawing predictive and coherence inferences during normal story comprehension
Brain Lang
 , 
2000
, vol. 
71
 (pg. 
310
-
36
)
Berlin
HA
Rolls
ET
Iversen
SD
Borderline personality disorder, impulsivity, and the orbitofrontal cortex
Am J Psychiatry
 , 
2005
, vol. 
162
 (pg. 
2360
-
73
)
Binder
JR
Rao
SM
Hammeke
TA
Yetkin
FZ
Jesmanowicz
A
Bandettini
PA
, et al.  . 
Functional magnetic resonance imaging of human auditory cortex
Ann Neurol
 , 
1994
, vol. 
35
 (pg. 
662
-
72
)
Black
FW
Cognitive deficits in patients with unilateral war-related frontal lobe lesions
J Clin Psychol
 , 
1976
, vol. 
32
 (pg. 
366
-
72
)
Blair
RJ
Cipolotti
L
Impaired social response reversal. A case of ‘acquired sociopathy’
Brain
 , 
2000
, vol. 
123
 
Pt 6
(pg. 
1122
-
41
)
Botvinick
MM
Braver
TS
Barch
DM
Carter
CS
Cohen
JD
Conflict monitoring and cognitive control
Psychol Rev
 , 
2001
, vol. 
108
 (pg. 
624
-
52
)
Brookshire
RH
Nicholas
LE
Comprehension of directly and indirectly stated main ideas and details in discourse by brain-damaged and non-brain-damaged listeners
Brain Lang
 , 
1984
, vol. 
21
 (pg. 
21
-
36
)
Brownell
H
Stringfellow
A
Making requests: illustrations of how right-hemisphere brain damage can affect discourse production
Brain Lang
 , 
1999
, vol. 
68
 (pg. 
442
-
65
)
Bugg
JM
Zook
NA
DeLosh
EL
Davalos
DB
Davis
HP
Age differences in fluid intelligence: contributions of general slowing and frontal decline
Brain Cogn
 , 
2006
, vol. 
62
 (pg. 
9
-
16
)
Burgess
PW
Shallice
T
Response suppression, initiation and strategy use following frontal lobe lesions
Neuropsychologia
 , 
1996
, vol. 
34
 (pg. 
263
-
72
)
Chiang
MC
Barysheva
M
Shattuck
DW
Lee
AD
Madsen
SK
Avedissian
C
, et al.  . 
Genetics of brain fiber architecture and intellectual performance
J Neurosci
 , 
2009
, vol. 
29
 (pg. 
2212
-
24
)
Chiappe
P
Hasher
L
Siegel
LS
Working memory, inhibitory control, and reading disability
Mem Cognit
 , 
2000
, vol. 
28
 (pg. 
8
-
17
)
Collins
DL
Neelin
P
Peters
TM
Evans
AC
Automatic 3D intersubject registration of MR volumetric data in standardized talairach space
J Comput Assist Tomo
 , 
1994
, vol. 
18
 (pg. 
192
-
205
)
Colom
R
Abad
FJ
Quiroga
MA
Shih
PC
Flores-Mendoza
C
Working memory and intelligence are highly related constructs, but why?
Intelligence
 , 
2008
, vol. 
36
 (pg. 
584
-
606
)
Colom
R
Haier
RJ
Head
K
Alvarez-Linera
J
Quiroga
MA
Shih
PC
, et al.  . 
Gray matter correlates of fluid, crystallized, and spatial intelligence: testing the P-FIT model
Intelligence
 , 
2009
, vol. 
37
 (pg. 
124
-
35
)
Costa
PT
Jr
McCrae
RR
Overview: innovations in assessment using the revised NEO personality inventory
Assessment
 , 
2000
, vol. 
7
 (pg. 
325
-
7
)
Crone
EA
Wendelken
C
Donohue
SE
Bunge
SA
Neural evidence for dissociable components of task-switching
Cereb Cortex
 , 
2006
, vol. 
16
 (pg. 
475
-
86
)
D'Esposito
M
Cooney
JW
Gazzaley
A
Gibbs
SE
Postle
BR
Is the prefrontal cortex necessary for delay task performance? Evidence from lesion and FMRI data
J Int Neuropsychol Soc
 , 
2006
, vol. 
12
 (pg. 
248
-
60
)
D'Esposito
M
Postle
BR
The dependence of span and delayed-response performance on prefrontal cortex
Neuropsychologia
 , 
1999
, vol. 
37
 (pg. 
1303
-
15
)
Dijk
TAv
Kintsch
W
Strategies of discourse comprehension
 , 
1983
New York
Academic Press
Dosenbach
NU
Visscher
KM
Palmer
ED
Miezin
FM
Wenger
KK
Kang
HC
, et al.  . 
A core system for the implementation of task sets
Neuron
 , 
2006
, vol. 
50
 (pg. 
799
-
812
)
Duncan
J
The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour
Trends Cogn Sci
 , 
2010
, vol. 
14
 (pg. 
172
-
9
)
Duncan
J
Burgess
P
Emslie
H
Fluid intelligence after frontal lobe lesions
Neuropsychologia
 , 
1995
, vol. 
33
 (pg. 
261
-
8
)
Diamond
A
Executive functions
Ann Rev Psychol
 , 
2013
, vol. 
64
 (pg. 
135
-
68
)
Egidi
G
Caramazza
A
Cortical systems for local and global integration in discourse comprehension
Neuroimage
 , 
2013
, vol. 
71
 (pg. 
59
-
74
)
Eslinger
PJ
Damasio
AR
Severe disturbance of higher cognition after bilateral frontal lobe ablation: patient EVR
Neurology
 , 
1985
, vol. 
35
 (pg. 
1731
-
41
)
Egidi
G
Nusbaum
HC
Emotional language processing: how mood affects integration processes during discourse comprehension
Brain Lang
 , 
2012
, vol. 
122
 (pg. 
199
-
210
)
Ferstl
EC
Neumann
J
Bogler
C
von Cramon
DY
The extended language network: a meta-analysis of neuroimaging studies on text comprehension
Hum Brain Mapp
 , 
2008
, vol. 
29
 (pg. 
581
-
93
)
Ferstl
EC
Rinck
M
von Cramon
DY
Emotional and temporal aspects of situation model processing during text comprehension: an event-related fMRI study
J Cogn Neurosci
 , 
2005
, vol. 
17
 (pg. 
724
-
39
)
Ferstl
EC
von Cramon
DY
The role of coherence and cohesion in text comprehension: an event-related fMRI study
Brain Res Cogn Brain Res
 , 
2001
, vol. 
11
 (pg. 
325
-
40
)
Ferstl
EC
von Cramon
DY
What does the frontomedian cortex contribute to language processing: coherence or theory of mind?
Neuroimage
 , 
2002
, vol. 
17
 (pg. 
1599
-
612
)
Fiez
JA
Petersen
SE
Neuroimaging studies of word reading
Proc Natl Acad Sci USA
 , 
1998
, vol. 
95
 (pg. 
914
-
21
)
Fletcher
PC
Happe
F
Frith
U
Baker
SC
Dolan
RJ
Frackowiak
RS
, et al.  . 
Other minds in the brain: a functional imaging study of ‘theory of mind’ in story comprehension
Cognition
 , 
1995
, vol. 
57
 (pg. 
109
-
28
)
Frith
U
Frith
CD
Development and neurophysiology of mentalizing
Philos Trans R Soc Lond B Biol Sci
 , 
2003
, vol. 
358
 (pg. 
459
-
73
)
Gerrig
RJ
Experiencing narrative worlds
 , 
1993
New Haven, CT
Yale University Press
Gernsbacher
MA
Language comprehension as structure building
 , 
1990
Hillsdale, NJ
L. Erlbaum
Giraud
AL
Truy
E
Frackowiak
RS
Gregoire
MC
Pujol
JF
Collet
L
Differential recruitment of the speech processing system in healthy subjects and rehabilitated cochlear implant patients
Brain
 , 
2000
, vol. 
123 (Pt 7)
 (pg. 
1391
-
402
)
Glascher
J
Rudrauf
D
Colom
R
Paul
LK
Tranel
D
Damasio
H
, et al.  . 
Distributed neural system for general intelligence revealed by lesion mapping
Proc Natl Acad Sci USA
 , 
2010
, vol. 
107
 (pg. 
4705
-
9
)
Glascher
J
Tranel
D
Paul
LK
Rudrauf
D
Rorden
C
Hornaday
A
, et al.  . 
Lesion mapping of cognitive abilities linked to intelligence
Neuron
 , 
2009
, vol. 
61
 (pg. 
681
-
91
)
Goldman
SR
Bloome
NS-FDM
Cognitive aspects of constructing meaning through and across multiple texts
Uses of intertextuality in classroom and educational research
 , 
2004
Greenwich, CT
Information Age Publishing
(pg. 
313
-
47
)
Hasson
U
Nusbaum
HC
Small
SL
Brain networks subserving the extraction of sentence information and its encoding to memory
Cereb Cortex
 , 
2007
, vol. 
17
 (pg. 
2899
-
913
)
Huettner
MI
Rosenthal
BL
Hynd
GW
Regional cerebral blood flow (rCBF) in normal readers: bilateral activation with narrative text
Arch Clin Neuropsychol
 , 
1989
, vol. 
4
 (pg. 
71
-
8
)
Isingrini
M
Vazou
F
Relation between fluid intelligence and frontal lobe functioning in older adults
Int J Aging Hum Dev
 , 
1997
, vol. 
45
 (pg. 
99
-
109
)
Johnson
HM
Seifert
CM
Sources of the continued influence effect: when misinformation in memory affects later inferences
J Exp Psychol Learn Mem Cogn
 , 
1994
, vol. 
20
 (pg. 
1420
-
36
)
Jung
RE
Haier
RJ
The Parieto-Frontal Integration Theory (P-FIT) of intelligence: converging neuroimaging evidence
Behav Brain Sci
 , 
2007
, vol. 
30
 (pg. 
135
-
54; discussion 54–87
)
Kane
MJ
Engle
RW
The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: an individual-differences perspective
Psychon Bull Rev
 , 
2002
, vol. 
9
 (pg. 
637
-
71
)
Kane
MJ
Hasher
L
Stoltzfus
ER
Zacks
RT
Connelly
SL
Inhibitory attentional mechanisms and aging
Psychol Aging
 , 
1994
, vol. 
9
 (pg. 
103
-
12
)
Koechlin
E
Basso
G
Pietrini
P
Panzer
S
Grafman
J
The role of the anterior prefrontal cortex in human cognition
Nature
 , 
1999
, vol. 
399
 (pg. 
148
-
51
)
Koenigs
M
Barbey
AK
Postle
BR
Grafman
J
Superior parietal cortex is critical for the manipulation of information in working memory
J Neurosci
 , 
2009
, vol. 
29
 (pg. 
14980
-
6
)
Komeda
H
Kawasaki
M
Tsunemi
K
Kusumi
T
Differences between estimating protagonists' emotions and evaluating readers' emotions in narrative comprehension
Cogn Emot
 , 
2009
, vol. 
23
 (pg. 
135
-
51
)
Kroger
JK
Sabb
FW
Fales
CL
Bookheimer
SY
Cohen
MS
Holyoak
KJ
Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity
Cereb Cortex
 , 
2002
, vol. 
12
 (pg. 
477
-
85
)
Maguire
EA
Frith
CD
Morris
RG
The functional neuroanatomy of comprehension and memory: the importance of prior knowledge
Brain
 , 
1999
, vol. 
122 (Pt 10)
 (pg. 
1839
-
50
)
Makale
M
Solomon
J
Patronas
NJ
Danek
A
Butman
JA
Grafman
J
Quantification of brain lesions using interactive automated software
Behav Res Methods Instrum Comput
 , 
2002
, vol. 
34
 (pg. 
6
-
18
)
Martinez
K
Burgaleta
M
Roman
FJ
Escorial
S
Shih
PC
Quiroga
MA
, et al.  . 
Can fluid intelligence be reduced to ‘simple’ short-term storage?
Intelligence
 , 
2011
, vol. 
39
 (pg. 
473
-
80
)
Mayer
JD
Salovey
P
Caruso
DR
Emotional intelligence: new ability or eclectic traits?
Am Psychol
 , 
2008
, vol. 
63
 (pg. 
503
-
17
)
Miller
EK
Cohen
JD
An integrative theory of prefrontal cortex function
Annu Rev Neurosci
 , 
2001
, vol. 
24
 (pg. 
167
-
202
)
Muller
NG
Machado
L
Knight
RT
Contributions of subregions of the prefrontal cortex to working memory: evidence from brain lesions in humans
J Cogn Neurosci
 , 
2002
, vol. 
14
 (pg. 
673
-
86
)
Nicholas
LE
Brookshire
RH
Consistency of the effects of rate of speech on brain-damaged adults' comprehension of narrative discourse
J Speech Hear Res
 , 
1986
, vol. 
29
 (pg. 
462
-
70
)
O'brien
EJ
Cook
AE
Gueraud
S
Accessibility of outdated information
J Exp Psychol Learn Mem Cogn
 , 
2010
, vol. 
36
 (pg. 
979
-
91
)
Ochsner
KN
Current directions in social cognitive neuroscience
Curr Opin Neurobiol
 , 
2004
, vol. 
14
 (pg. 
254
-
8
)
Ochsner
KN
Lieberman
MD
The emergence of social cognitive neuroscience
Am Psychol
 , 
2001
, vol. 
56
 (pg. 
717
-
34
)
Owen
AM
McMillan
KM
Laird
AR
Bullmore
E
N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies
Hum Brain Mapp
 , 
2005
, vol. 
25
 (pg. 
46
-
59
)
Parkin
AJ
Java
RI
Deterioration of frontal lobe function in normal aging: influences of fluid intelligence versus perceptual speed
Neuropsychology
 , 
1999
, vol. 
13
 (pg. 
539
-
45
)
Patterson
R
Barbey
AK
Grafman
J
Krueger
F
A cognitive neuroscience framework for causal reasoning
The Neural Representation of Belief Systems
 , 
2012
New York
Psychology Press
(pg. 
76
-
120
)
Payne
BR
Gao
X
Noh
SR
Anderson
CJ
Stine-Morrow
EA
The effects of print exposure on sentence processing and memory in older adults: evidence for efficiency and reserve
Neuropsychol Dev Cogn B Aging Neuropsychol Cogn
 , 
2012
, vol. 
19
 (pg. 
122
-
49
)
Ramnani
N
Owen
AM
Anterior prefrontal cortex: insights into function from anatomy and neuroimaging
Nat Rev Neurosci
 , 
2004
, vol. 
5
 (pg. 
184
-
94
)
Rapp
DN
van den Broek
P
Dynamic text comprehension: an integrative view of reading
Curr Dir Psychol Sci
 , 
2005
, vol. 
14
 (pg. 
276
-
9
)
Raymont
V
Salazar
AM
Lipsky
R
Goldman
D
Tasick
G
Grafman
J
Correlates of posttraumatic epilepsy 35 years following combat brain injury
Neurology
 , 
2010
, vol. 
75
 (pg. 
224
-
9
)
Raz
N
Dahle
CL
Rodrigue
KM
Kennedy
KM
Land
S
Effects of age, genes, and pulse pressure on executive functions in healthy adults
Neurobiol Aging
 , 
2011
, vol. 
32
 (pg. 
1124
-
37
)
Robertson
DA
Gernsbacher
MA
Guidotti
SJ
Robertson
RR
Irwin
W
Mock
BJ
, et al.  . 
Functional neuroanatomy of the cognitive process of mapping during discourse comprehension
Psychol Sci
 , 
2000
, vol. 
11
 (pg. 
255
-
60
)
Robertson
LC
Lamb
MR
Knight
RT
Effects of lesions of temporal-parietal junction on perceptual and attentional processing in humans
J Neurosci
 , 
1988
, vol. 
8
 (pg. 
3757
-
69
)
Roca
M
Parr
A
Thompson
R
Woolgar
A
Torralva
T
Antoun
N
, et al.  . 
Executive function and fluid intelligence after frontal lobe lesions
Brain
 , 
2010
, vol. 
133 (Pt 1)
 (pg. 
234
-
47
)
Rouet
JF
The skills of document use: from text comprehension to web-based learning
 , 
2006
Mahwah
Erlbaum
Sabbagh
MA
Understanding orbitofrontal contributions to theory-of-mind reasoning: implications for autism
Brain Cogn
 , 
2004
, vol. 
55
 (pg. 
209
-
19
)
Saxe
R
Uniquely human social cognition
Curr Opin Neurobiol
 , 
2006
, vol. 
16
 (pg. 
235
-
9
)
Shallice
T
Burgess
PW
Deficits in strategy application following frontal lobe damage in man
Brain
 , 
1991
, vol. 
114
 
Pt 2
(pg. 
727
-
41
)
Smiler
AP
Gagne
DD
Stine-Morrow
EA
Aging, memory load, and resource allocation during reading
Psychol Aging
 , 
2003
, vol. 
18
 (pg. 
203
-
9
)
Solomon
J
Raymont
V
Braun
A
Butman
JA
Grafman
J
User-friendly software for the analysis of brain lesions (ABLe)
Comput Methods Programs Biomed
 , 
2007
, vol. 
86
 (pg. 
245
-
54
)
Sparks
JR
Rapp
DN
Readers' reliance on source credibility in the service of comprehension
J Exp Psychol Learn Mem Cogn
 , 
2011
, vol. 
37
 (pg. 
230
-
47
)
St George
M
Kutas
M
Martinez
A
Sereno
MI
Semantic integration in reading: engagement of the right hemisphere during discourse processing
Brain
 , 
1999
, vol. 
122
 
Pt 7
(pg. 
1317
-
25
)
Stemmer
B
Whitaker
HA
Handbook of the neuroscience of language
 , 
2008
1st edn
Amsterdam; Boston
Academic Press/Elsevier
Stoltzfus
ER
Hasher
L
Zacks
RT
Ulivi
MS
Goldstein
D
Investigations of inhibition and interference in younger and older adults
J Gerontol
 , 
1993
, vol. 
48
 (pg. 
P179
-
88
)
Stowe
LA
Broere
CA
Paans
AM
Wijers
AA
Mulder
G
Vaalburg
W
, et al.  . 
Localizing components of a complex task: sentence processing and working memory
Neuroreport
 , 
1998
, vol. 
9
 (pg. 
2995
-
9
)
Theide
KW
Griffin
TD
Wiley
J
Andersen
MCM
Poor metacomprehension accuracy as a result of inappropriate cue use
Discourse Processes
 , 
2010
, vol. 
47
 (pg. 
331
-
62
)
Tsuchida
A
Fellows
LK
Lesion evidence that two distinct regions within prefrontal cortex are critical for n-back performance in humans
J Cogn Neurosci
 , 
2009
, vol. 
21
 (pg. 
2263
-
75
)
Turkeltaub
PE
Eden
GF
Jones
KM
Zeffiro
TA
Meta-analysis of the functional neuroanatomy of single-word reading: method and validation
Neuroimage
 , 
2002
, vol. 
16
 
3 Pt 1
(pg. 
765
-
80
)
Tzourio-Mazoyer
N
Landeau
B
Papathanassiou
D
Crivello
F
Etard
O
Delcroix
N
, et al.  . 
Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain
Neuroimage
 , 
2002
, vol. 
15
 (pg. 
273
-
89
)
Vigneau
M
Beaucousin
V
Herve
PY
Duffau
H
Crivello
F
Houde
O
, et al.  . 
Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing
Neuroimage
 , 
2006
, vol. 
30
 (pg. 
1414
-
32
)
Vogeley
K
Bussfeld
P
Newen
A
Herrmann
S
Happe
F
Falkai
P
, et al.  . 
Mind reading: neural mechanisms of theory of mind and self-perspective
Neuroimage
 , 
2001
, vol. 
14
 
1 Pt 1
(pg. 
170
-
81
)
Volle
E
Kinkingnehun
S
Pochon
JB
Mondon
K
Thiebaut de Schotten
M
Seassau
M
, et al.  . 
The functional architecture of the left posterior and lateral prefrontal cortex in humans
Cereb Cortex
 , 
2008
, vol. 
18
 (pg. 
2460
-
9
)
Wager
TD
Smith
EE
Neuroimaging studies of working memory: a meta-analysis
Cogn Affect Behav Neurosci
 , 
2003
, vol. 
3
 (pg. 
255
-
74
)
Wechsler
D
Wechsler adult intelligence test administration and scoring manual
 , 
1997
San Antonio, TX
The Psychology Corporation
Wegner
ML
Brookshire
RH
Nicholas
LE
Comprehension of main ideas and details in coherent and noncoherent discourse by aphasic and nonaphasic listeners
Brain Lang
 , 
1984
, vol. 
21
 (pg. 
37
-
51
)
Wineburg
SS
Historical thinking and other unnatural acts: charting the future of teaching the past
 , 
2001
Philadelphia
Temple University Press
Winner
E
Brownell
H
Happe
F
Blum
A
Pincus
D
Distinguishing lies from jokes: theory of mind deficits and discourse interpretation in right hemisphere brain-damaged patients
Brain Lang
 , 
1998
, vol. 
62
 (pg. 
89
-
106
)
Wolf
RC
Thomann
PA
Sambataro
F
Vasic
N
Schmid
M
Wolf
ND
Orbitofrontal cortex and impulsivity in borderline personality disorder: an MRI study of baseline brain perfusion
Eur Arch Psychiatry Clin Neurosci
 , 
2012
, vol. 
262
 (pg. 
677
-
85
)
Woods
RP
Mazziotta
JC
Cherry
SR
MRI-PET registration with automated algorithm
J Comput Assist Tomogr
 , 
1993
, vol. 
17
 (pg. 
536
-
46
)
Woolgar
A
Parr
A
Cusack
R
Thompson
R
Nimmo-Smith
I
Torralva
T
, et al.  . 
Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex
Proc Natl Acad Sci USA
 , 
2010
, vol. 
107
 (pg. 
14899
-
902
)
Xu
J
Kemeny
S
Park
G
Frattali
C
Braun
A
Language in context: emergent features of word, sentence, and narrative comprehension
Neuroimage
 , 
2005
, vol. 
25
 (pg. 
1002
-
15
)
Zwaan
RA
Radvansky
GA
Situation models in language comprehension and memory
Psychol Bull
 , 
1998
, vol. 
123
 (pg. 
162
-
85
)