Elsevier

NeuroImage

Volume 29, Issue 1, 1 January 2006, Pages 254-266
NeuroImage

Cognitive modules utilized for narrative comprehension in children: a functional magnetic resonance imaging study

https://doi.org/10.1016/j.neuroimage.2005.07.020Get rights and content

Abstract

The ability to comprehend narratives constitutes an important component of human development and experience. The neural correlates of auditory narrative comprehension in children were investigated in a large-scale functional magnetic resonance imaging (fMRI) study involving 313 subjects ages 5–18. Using group independent component analysis (ICA), bilateral task-related components were found comprising the primary auditory cortex, the mid-superior temporal gyrus, the hippocampus, the angular gyrus, and medial aspect of the parietal lobule (precuneus/posterior cingulate). In addition, a right-lateralized component was found involving the most posterior aspect of the superior temporal gyrus, and a left-lateralized component was found comprising the inferior frontal gyrus (including Broca's area), the inferior parietal lobule, and the medial temporal gyrus. Using a novel data-driven analysis technique, increased task-related activity related to age was found in the components comprising the mid-superior temporal gyrus (Wernicke's area) and the posterior aspect of the superior temporal gyrus, while decreased activity related to age was found in the component comprising the angular gyrus. The results are discussed in light of recent hypotheses involving the functional segregation of Wernicke's area and the specific role of the mid-superior temporal gyrus in speech comprehension.

Introduction

During the early school years, school performance is significantly impacted by story comprehension skills (Lorch et al., 1998). Children's ability to comprehend fictional narratives is related to three key aspects of the story: the causal relationships in stories, the goals and internal states of the characters in the stories, and the integration of the different parts of the stories (Trabasso and Stein, 1997, Van den Broek, 1997). The listener (or reader) has the expectation of logical coherence (cause and effect) between events (Barthes, 1981, Graesser et al., 1980). However, often the inference of specific intentions, goals, or mental/emotional states for a specific character in the narrative is necessary for the listener to properly construct causal relationships (Frith and Frith, 1999, Gernsbacher et al., 1992, Oatley, 1992, Peterson, 1999). Therefore, comprehension of narratives involves more than comprehension of the individual sentences that comprise the story.

Previous neuroimaging studies of simple narrative comprehension have yielded conflicting results. A functional magnetic resonance imaging (fMRI) study (Vogeley et al., 2001) yielded no increase in neuronal activation during reading of “physical” stories without an element of “theory-of-mind” (predicting the behavior of others by means of their mental states; Frith et al., 1991, Happe et al., 1996) versus a baseline condition of the reading of unlinked sentences. However, an earlier positron emission tomography (PET) study (Fletcher et al., 1995) did show activation increases in the temporal poles bilaterally, the left superior temporal gyrus and the posterior cingulate cortex for the same functional contrast (reading physical stories versus unlinked sentences). Activation increases in similar regions were observed in a separate PET study (Mazoyer et al., 1993) investigating auditory narrative comprehension (listening to stories in native language versus an unknown foreign language). It has been suggested (Mar, 2004) that the discrepancy in results may be due to methodological differences (imaging method and threshold set for statistical significance) as well as a different baseline task: Vogeley et al. used unlinked sentences as a control task, which may mask some activation, as the subjects will likely attempt to make sense of each sentence individually.

To investigate the neural correlates of auditory sentence processing and narrative comprehension in children, we performed a large-scale study using fMRI involving subjects ages 5–18 years old. The stories presented were simple stories, without an element of “theory-of-mind”, and were quite short, obviating the necessity of higher-order integrative processes (e.g., between groups of events) in order make the difficulty level suitable for young children. In addition to activation in primary auditory areas, we predict, based on previous results (Fletcher et al., 1995, Gallagher et al., 2000, Mazoyer et al., 1993), that the task of auditory narrative processing will recruit the superior temporal gyrus, posterior cingulate gyrus, and inferior parietal lobules, as well as areas recruited for semantic and syntactic elements of language processing such as the angular gyrus and inferior frontal gyrus (Fiebach et al., 2005, Holland et al., 2001).

Since we wished to investigate the neural correlates of macro-level (e.g., recognition of causal relationships in the stories) processes as well as micro-level (e.g., words and sentences) language processes, we selected group independent component analysis (ICA) (Calhoun et al., 2001, McKeown et al., 1998, Schmithorst and Holland, 2004) as our data analysis technique. Group ICA has the advantage that the design matrix or hemodynamic response functions (HRFs) need not be specified a priori and are allowed to vary across subjects. This is important for the investigation of macro-level processes as the HRF may have considerable variance across subjects as well as not correlate well with the typical regressor used in the general linear model (GLM) (Worsley and Friston, 1995) approach (e.g., a square wave convolved with an impulse HRF). Group ICA analysis has been previously used for a variety of fMRI studies including those investigating math processing (Schmithorst and Brown, 2004), alcohol intoxication effects on simulated driving (Calhoun et al., 2004b), and music perception (Schmithorst, 2005).

Section snippets

Materials and methods

313 children (152 boys, 161 girls) were successfully scanned as part of this study following Institutional Review Board approval and informed consent by the child's parent or guardian (assent was also obtained from subjects eight years and older). Exclusion criteria were as follows: previous neurological illness, learning disability, head trauma with loss of consciousness, current or past use of psychostimulant medication, pregnancy, birth at 37 weeks gestational age or earlier, or abnormal

Results

Performance data for post-scan recall were available from 307 out of the 313 subjects scanned. 267 out of the 307 subjects (or 87% of the study population) answered at least 6 out of the 10 questions correctly (corresponding to P < 0.02 for responding at a chance level). No significant performance difference was seen between boys and girls (P > 0.39, chi-squared contingency test). However, significant effects for subject age (Spearman's R = 0.28, P < 0.001), full-scale IQ (Spearman's R = 0.26, P

Discussion

Spatial ICA reveals “chronoarchitectonically identified areas” (Bartels and Zeki, 2004) or functionally connected regions. The presence of different cortical regions in the same ICA component implies that they are active at the same time (subject to the limitations of the temporal resolution of the fMRI data acquisition); otherwise, the ICA algorithm would have separated them out into different components. ICA provides different information than other techniques such as diffusion tensor imaging

Conclusion

A large-scale fMRI study of auditory narrative comprehension was conducted on a group of over 300 children ages 5–18. Using group ICA analysis, separate task-related networks were detected, including the primary auditory cortex bilaterally, mid-superior temporal gyrus bilaterally, hippocampus bilaterally, a left-lateralized network including Broca's area and the left inferior parietal lobule, a slightly right-lateralized network involving the posterior superior temporal gyri, and a bilateral

Acknowledgments

This work was supported by a grant from the U.S. National Institute of Child Health and Human Development, #R01-HD38578. The authors acknowledge the assistance of Dr. Anna Byars, PhD, in the administration of the Wechsler Full-Scale IQ tests; and of Drs. Richard Strawsburg, MD, and Mark Schapiro, MD, for performing the neurological examinations.

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