Narrative speech production: An fMRI study using continuous arterial spin labeling☆,☆☆
Introduction
Narrative production involves organizing and expressing a complex series of events. This process is fundamental for human communication, yet we know little about its neural basis. Our model of narrative production involves at least two components, including a linguistic component and an executive resource component (Mar, 2004). Linguistic functions implicated during narrative production include phonology, morphology, lexical, and grammatical processing, which serve to express the content of a story. The focus of this study is the second component, involving higher-level cognitive processes that play a crucial role in organizing a narrative, such as sustaining a story’s theme through working memory, and maintaining story coherence through top–down planning and organization. These linguistic and cognitive processes must successfully interact to produce a sequence of utterances that relate to each other in expressing a logical and coherent narrative. In this report, we use functional magnetic resonance imaging (fMRI) with continuous arterial spin labeling (CASL) to monitor regional brain activation during narrative speech production.
Observations of non-aphasic patients with focal central nervous system damage implicate frontal cortex in the higher-level processes contributing to narrative. For example, patients with executive dysfunction due to prefrontal damage following traumatic brain injury fail to construct cohesive, temporally sequenced speech samples (Ferstl et al., 1999, Ferstl and von Cramon, 2002). This dysfunction can appear after damage to left or right prefrontal cortex. Patients with Alzheimer’s disease also have narrative deficits (Chapman et al., 2002, Glosser and Deser, 1992). Deficits in narrative production in AD have also been attributed to executive dysfunction, although their episodic memory difficulty makes it difficult to determine the basis for their poor narrative performance.
Perhaps the most informative studies come from non-aphasic patients with frontotemporal dementia (FTD) who have social and executive limitations but minor memory impairments (Libon et al., 2007). These patients experience significant narrative difficulty (Ash et al., 2006, Chapman et al., 2005). A detailed analysis of performance when narrating a wordless picture story shows that these patients have a limited grasp of the story’s overall theme and poor connectedness between specific events in their stories, even though lexical and grammatical aspects of word and sentence use are relatively preserved (Ash et al., 2006). Additional evidence consistent with impaired top–down organization comes from a selective deficit at detecting errors in the ordering of script events in these social and executive FTD patients, and their greater deficit with event ordering than the detection of semantic substitutions in a script (Cosentino et al., 2006). FTD patients with social and executive deficits tend to have cortical atrophy in prefrontal, ventral frontal, and anterior temporal brain regions, often more prominently on the right than the left (Grossman et al., 2004, Rosen et al., 2005, Williams et al., 2005). Direct evidence relating narrative limitations to a specific neuroanatomic substrate comes from a correlative study of these non-aphasic FTD patients. Using a voxel-based morphometric analysis of cortical volume, Ash et al. (2006) observed a specific correlation between limited connectedness in story narrative and cortical atrophy in prefrontal, inferior frontal, and temporal regions of FTD patients.
In the current study, we sought converging evidence about the neural basis for narrative discourse in healthy young adults from fMRI. Several studies have used fMRI to monitor the appreciation of narrative coherence, finding that bilateral medial and lateral frontal and anterior temporal regions are activated while listening to a narrative relative to baselines involving rest or unrelated sentences (Fletcher et al., 1995, Gallagher, 2000, Mazoyer et al., 1993, Xu et al., 2005). A more explicit approach to the evaluation of narrative reported left medial prefrontal activation during explicit judgments of the coherence of pairs of sentences (Ferstl and von Cramon, 2002) or coherence judgments depending on the presence of definite articles (Robertson et al., 2000). In two recent studies, subjects were asked to judge the relatedness of a third sentence to two prior sentences establishing the scene (Kuperberg et al., 2006, Mason and Just, 2004). This work reported bilateral frontal, temporal, and parietal activation that was greatest for stimuli demanding a coherent linkage between sentences.
We were particularly interested in monitoring regional brain activity during a more natural and ecologically valid task than passively listening to narrative – narrative speech production. One strategy for studying narrative production involves examining activation during inner speech (Wildgruber et al., 1996, Wildgruber et al., 2001). The results of studies involving inner speech are often compatible with those involving actual speech production (Palmer et al., 2001, Rosen et al., 2000, Shuster and Lemieux, 2005), although this work has focused on single words. Moreover, we wanted to ensure that we were monitoring brain activity during coherent, full narrative production where discourse organization must be explicit rather than during a kind of mental shorthand where organizational links crucial to the coherence of a narrative may not be fully realized. We also sought to minimize the methodological confound of the absence of auditory self-stimulation during the production of silent inner speech, and we wanted to be able to monitor narrative accuracy (Munhall, 2001).
Monitoring brain activity during speech requires us to limit motion artifact. In one influential study looking at narrative production, activity was monitored during an extended speech sample with PET (Braun et al., 2001). A broad range of brain regions was activated during subjects’ extemporaneous accounts of personal experiences. Among these were inferior, dorsolateral, and medial frontal regions as well as lateral temporal regions, more prominently on the left than on the right, and bilateral temporal–occipital regions. Since narratives were produced with both oral speech and gestural sign language in this study, activations seen in this conjunction analysis were common to both modalities and thus could not be easily attributed to modality-specific components such as a motor speech mechanism. This study is extraordinarily important because of its ecological validity, but the target of the narrative was not known and thus the ability to validate the content of the narrative was limited.
Additional reports describe studies of speech production during fMRI (Palmer et al., 2001, Rosen et al., 2000, Shuster and Lemieux, 2005). fMRI has many advantages over PET due to its superior spatial resolution, non-invasiveness, and absence of ionizing radiation. However, many challenges must be overcome during the collection of speech data in the bore of a magnet (Birn et al., 2004, Xu et al., 2005). These are due to facial muscle and tongue use, head movement, and other artifact-producing aspects of speech production. Moreover, we sought to collect data over an extended period of time, i.e., in a manner that more closely resembles the extended narrative discourse that we use in our day-to-day speech. This was achieved by asking participants to formulate a narrative consisting of an extended speech sample based on a large sequence of pictures illustrating a children’s picture story. We circumvented potential problems associated with fMRI data collection during speech by using sparse data sampling, taking advantage of the delay in the hemodynamic response to collect cortical activation data following the cessation of speech (Belin et al., 1998, Hall et al., 1999). We also elected to use perfusion fMRI based on an arterial spin labeling (ASL) perfusion technique rather than blood oxygen level-dependent (BOLD) fMRI because ASL contrast does not depend on susceptibility effects, and ASL perfusion fMRI can be obtained using imaging sequences that minimize artifacts from static susceptibility gradients (Fernández-Seara et al., 2005, Kemeny et al., 2005, Kim et al., 2006). Further, because labeled and control images are interleaved during ASL scanning, ASL perfusion fMRI data do not suffer from the low-frequency noise that is typically present in BOLD data, and sustained task conditions can be studied without any penalty (Wang et al., 2003).
Finally, we attempted to devise baseline conditions that would allow us to separate the top–down organization component of extended narrative apart from factors like the meaningfulness of the language being produced, the gist level of narrative appreciation associated with an approximation of story organization, and the stimulation associated with hearing one’s own voice. Our first baseline involved the description of single pictures that could not be assembled into an extended narrative. This allowed us to control for grammatical, phonologic, and lexical semantic content of speech while minimizing the narrative component involved in describing the story associated with a long series of pictures. The second baseline involved looking at the ordered pictures of the entire story while producing a nonsense word to control for low-level motor components of articulation and suppress executive resources associated with inner speech such as the phonologic loop of working memory. Based on our previous experience with correlative studies of narrative speech deficits with frontal cortical atrophy in FTD (Ash et al., 2006) and previous studies of narrative speech in a PET environment (Braun et al., 2001), we hypothesized that we would see activations consistent with our two-component model of narrative, including bilateral frontal activation to support narrative organization and temporal–parietal activation to support story content during narrative expression.
Section snippets
Subjects
Participants included 15 healthy, right-handed, native English speakers (10 females and 5 males, mean age = 24.4 years; mean education = 15.8 years) from the University of Pennsylvania community who were paid for their participation. They completed an informed consent procedure approved by the Institutional Review Board at the University of Pennsylvania.
Materials
We elicited a semi-structured speech sample from the subjects with the wordless children’s picture book, Frog, Where Are You (Mayer, 1969). The
Behavioral results
Means of coded variables for each block can be found in Table 1. The Wilcoxon rank sum test was used to examine differences between blocks. The P-value is reported whenever it is less than 0.05. The narrative production block contained significantly more narrative elements than the picture description block (p < .001). Otherwise, there were no significant differences between the coded variables of total words, syntax, or syllables between these two blocks.
Imaging results
Table 2 summarizes the peak activations
Discussion
Narrative production is a complex process involving at least two major components. Phonological, morphological, and semantic processes are important for the production of single words and the expression of story content. Story content itself is supported by perisylvian language regions, and visual and multimodal association cortices. Forming these words into a coherent sentence requires grammatical processing, and combining sentences into a narrative that conveys meaning calls for the
Conclusion
With these caveats in mind, a large network appears to be recruited during speech production to help organize and express a coherent narrative. This includes inferior frontal cortex bilaterally, as well as dorsal frontal, temporal–parietal, and temporal–occipital regions of the left hemisphere. Inferior frontal regions appear to be important for supporting the organizational component of a narrative, while dorsal frontal areas may support working memory; temporal–parietal–occipital regions may
Acknowledgment
This work was supported in part by the National Institutes of Health (AG17586, NS44266, AG15116, NS53488).
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2017, NeuropsychologiaCitation Excerpt :Lesions to the right frontal lobe including the dorsolateral prefrontal cortex, both the anterior and superior temporal gyrus, the middle temporal gyrus, and the supramarginal gyrus were linked to poor performance in narrative complexity. Consistent with our findings, several fMRI studies investigating processing of narrative coherence showed greater activation in bilateral medial and lateral frontal and anterior temporal and left medial prefrontal regions (Ferstl et al., 2002; Fletcher et al., 1995; Gallagher et al., 2000; Mazoyer et al., 1993; Xu, Kemeny, Park, Frattali, and Braun, 2005, Troiani et al., 2008). Coelho and colleagues (2012) also reported that individuals with left DLPFC lesions have deficits in inclusion of critical story components and in global coherence.
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Portions of this work were presented at the American Academy of Neurology Annual Meeting, Boston, 2007.
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This work was supported in part by NIH (AG17586, AG15116, NS44266, NS53488, RR002305, BCS0517935, and the Dana Foundation).