Spotlights
Trends in Cognitive Sciences March 2014, Vol. 18, No. 3
Default mode network: the seat of literary creativity? Richard J.S. Wise1 and Rodrigo M. Braga1,2 1
Computational, Cognitive, and Clinical Neuroimaging Laboratory, Division of Brain Sciences, Imperial College, Hammersmith Hospital Campus, London W12 0NN, UK 2 MRC Clinical Sciences Centre, Commonwealth Building, Imperial College, Hammersmith Hospital Campus, London W12 0NN, UK
Literacy implies convergence, with heard and read narratives directed from separate sensory pathways towards common linguistic and semantic brain systems – very ‘bottom-up’. But we also actively infer, relate, remember, attend and, above all, imagine – very ‘topdown’. We comment on an interesting investigation of the listening and reading brain. Functional neuroimaging studies of language are popular. As an example, the meta-analysis by Vigneau and colleagues plotted 730 activation peaks from 129 separate language studies on to the left lateral cerebral hemisphere [1]. Most studies had required their participants to make decisions about specified linguistic or semantic properties of verbal stimuli. The many peaks were parceled into three groups, summarized as the functional anatomies of phonology, semantics, and syntax. They were largely confined to generously sized Broca’s and Wernicke’s areas. Regev and colleagues have recently published a study [2], using functional magnetic resonance imaging (fMRI), offering a very different perspective on the response of the brain during language comprehension. In design it is almost identical to a previous study except in the choice of scanning modality [3]; Spitsyna and colleagues used positron emission tomography (PET). Thus, both studies employed spoken and written narratives, with baseline stimuli of normal speech manipulated to retain its acoustic complexity while rendering it unintelligible and arrays of unreadable letter-like strings. Both made a point of avoiding metalinguistic task demands. The emphasis in the earlier study [3] was to identify where the two language streams converge on a proposed semantic ‘hub’. Convergence was defined as voxels activated by both spoken and written narratives relative to their respective baseline conditions. One view from the clinical and imaging literature on the neurodegenerative condition known as semantic dementia [4] locates this ‘hub’ in the rostral ventral left temporal lobe. Unlike fMRI as conventionally employed, with a blind spot due to magnetic field inhomogeneities, PET imaging can see this region. The PET study [3] duly demonstrated this to be one of the main sites of convergence. Corresponding author: Wise, R.J.S. ([email protected]). 1364-6613/$ – see front matter ß 2013 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.tics.2013.11.001
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By contrast, the results from the recent fMRI study [2] were discussed less in terms of convergence of different processing streams and more on what were termed selective and invariant neural responses. The method used to determine these responses was to extract the time courses of the low frequency fMRI signal across the 7 min of an unfolding narrative. The responses to the identical spoken and written versions were obtained from different participants, and at each voxel these responses were correlated across participants. In some regions, intersubject correlations were selective for one or other sensory modality, predictably most evident in unimodal auditory and visual cortex. In other regions, the intersubject correlations were significant across modalities. Observing invariant responses was only made possible by presenting the written narratives in an unusual way: as one or only a few words at a time in the center of the screen, with the timing imposed by the spoken version of the narrative. The authors were intrigued by relatively selective responses that they observed in frontoparietal networks, challenging ‘the classical distinction between sensory unimodal and higher-order amodal areas’. However, the interpretation of these dissociations is not straightforward. They may be the consequence of a partial dissociation of auditory and visual networks for attention [5], one of the suggestions put forward by the authors; but that is to overlook the natural presentation of the spoken narrative compared with the unnatural manner in which the written version had to be read. Thus, for example, a prominent right frontoparietal activity that was observed for the written relative to the spoken narrative was arguably a consequence of the relatively greater demand on sustained attention; in other words, activity associated with experimental design and not with language modality. We found the distribution of the invariant responses to be much more intriguing. Most prominent was a distribution of correlated activity in the midline posterior cortex and bilateral posterior inferior parietal cortex. This forms the posterior part of the so-called default mode network (DMN; Figure 1), a system classically associated with the introspective mind. It has been observed before, in another meta-analysis of language studies, one that set out to reveal the semantic system [6]. The authors of that review, and others since (e.g., [7]), have discussed how memories, semantic and personal, emotions, theory of mind, and no doubt many other mental functions are linked through the DMN. This would suggest that overlapping components of the DMN are functionally interconnected with many separate
Spotlights
Trends in Cognitive Sciences March 2014, Vol. 18, No. 3
whereas the study by Spitsyna made no such demand on the participants in their PET study. There is nothing like the threat of an examination to concentrate one’s mind – and maximize one’s brain activity. The recent result addresses the literary as opposed to simply the lingual brain. There is a longstanding and often ill-tempered debate about whether Shakespeare actually wrote, singly or as a co-author, the 37 plays attributed to him. It is argued that only a well-travelled Tudor aristocrat, versed in the ways of courtly love, would have had the experiences to write the histories, tragedies, and romantic comedies attributed to Shakespeare. Now we can speculate that some background reading and curiosity about the motivations of others, coupled with a spectacularly wellconnected DMN, made the bard immortal despite his humble origins. And we know that the DMN is as active in narrative production as it is in comprehension [10].
IPP
PCC
TRENDS in Cognitive Sciences
Figure 1. Spot the literary network: the default mode network (DMN) viewed from different angles (colors are intended for illustrative purposes only; data from [9]). The medial posterior cingulate (PCC) and inferior posterior parietal components (IPP) were implicated in linguistic processing by Regev et al. [2], but we suggest that due to the widespread connectivity of the DMN, these regions are related to higher order ‘literary’ processing.
brain systems, including those for language and semantics, and indeed this is turning out to be the case [8–10]. So why did the study of Spitsyna and colleagues [3] not reveal convergence within the DMN? The answer is it did, in a figure of statistically unthresholded analyses of the contrasts between the spoken and written narratives and their respective baseline conditions. The PET study was underpowered to reveal this activity at a thresholded level, but a further factor was likely to have been the expectations of the participants. In the study of Regev and colleagues [2] the participants knew they would have to recall the content of the narrative at the cessation of scanning,
References 1 Vigneau, M. et al. (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30, 1414–1432 2 Regev, M. et al. (2013) Selective and invariant neural responses to spoken and written narratives. J. Neurosci. 33, 15978–15988 3 Spitsyna, G. et al. (2006) Converging language streams in the human temporal lobe. J. Neurosci. 26, 7328–7336 4 Acosta-Cabronero, J. et al. (2011) Atrophy, hypometabolism and white matter abnormalities in semantic dementia tell a coherent story. Brain 134, 2025–2035 5 Braga, R.M. et al. (2013) Separable networks for top-down attention to auditory non-spatial and visuospatial modalities. Neuroimage 74, 77–86 6 Binder, J.R. et al. (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 19, 2767–2796 7 Buckner, R.L. and Carroll, D.C. (2007) Self-projection and the brain. Trends Cogn. Sci. 11, 49–57 8 Smith, S.M. et al. (2012) Temporally-independent functional modes of spontaneous brain activity. Proc. Natl. Acad. Sci. U.S.A. 109, 3131–3136 9 Braga, R.M. et al. (2013) Echoes of the brain within default mode, association, and heteromodal cortices. J. Neurosci. 33, 14031–14039 10 Awad, M. et al. (2007) A common system for the comprehension and production of narrative speech. J. Neurosci. 27, 11455–11464
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Trends in Cognitive Sciences March 2014, Vol. 18, No. 3
Default mode network: the seat of literary creativity? Richard J.S. Wise1 and Rodrigo M. Braga1,2 1
Computational, Cognitive, and Clinical Neuroimaging Laboratory, Division of Brain Sciences, Imperial College, Hammersmith Hospital Campus, London W12 0NN, UK 2 MRC Clinical Sciences Centre, Commonwealth Building, Imperial College, Hammersmith Hospital Campus, London W12 0NN, UK
Literacy implies convergence, with heard and read narratives directed from separate sensory pathways towards common linguistic and semantic brain systems – very ‘bottom-up’. But we also actively infer, relate, remember, attend and, above all, imagine – very ‘topdown’. We comment on an interesting investigation of the listening and reading brain. Functional neuroimaging studies of language are popular. As an example, the meta-analysis by Vigneau and colleagues plotted 730 activation peaks from 129 separate language studies on to the left lateral cerebral hemisphere [1]. Most studies had required their participants to make decisions about specified linguistic or semantic properties of verbal stimuli. The many peaks were parceled into three groups, summarized as the functional anatomies of phonology, semantics, and syntax. They were largely confined to generously sized Broca’s and Wernicke’s areas. Regev and colleagues have recently published a study [2], using functional magnetic resonance imaging (fMRI), offering a very different perspective on the response of the brain during language comprehension. In design it is almost identical to a previous study except in the choice of scanning modality [3]; Spitsyna and colleagues used positron emission tomography (PET). Thus, both studies employed spoken and written narratives, with baseline stimuli of normal speech manipulated to retain its acoustic complexity while rendering it unintelligible and arrays of unreadable letter-like strings. Both made a point of avoiding metalinguistic task demands. The emphasis in the earlier study [3] was to identify where the two language streams converge on a proposed semantic ‘hub’. Convergence was defined as voxels activated by both spoken and written narratives relative to their respective baseline conditions. One view from the clinical and imaging literature on the neurodegenerative condition known as semantic dementia [4] locates this ‘hub’ in the rostral ventral left temporal lobe. Unlike fMRI as conventionally employed, with a blind spot due to magnetic field inhomogeneities, PET imaging can see this region. The PET study [3] duly demonstrated this to be one of the main sites of convergence. Corresponding author: Wise, R.J.S. ([email protected]). 1364-6613/$ – see front matter ß 2013 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.tics.2013.11.001
116
By contrast, the results from the recent fMRI study [2] were discussed less in terms of convergence of different processing streams and more on what were termed selective and invariant neural responses. The method used to determine these responses was to extract the time courses of the low frequency fMRI signal across the 7 min of an unfolding narrative. The responses to the identical spoken and written versions were obtained from different participants, and at each voxel these responses were correlated across participants. In some regions, intersubject correlations were selective for one or other sensory modality, predictably most evident in unimodal auditory and visual cortex. In other regions, the intersubject correlations were significant across modalities. Observing invariant responses was only made possible by presenting the written narratives in an unusual way: as one or only a few words at a time in the center of the screen, with the timing imposed by the spoken version of the narrative. The authors were intrigued by relatively selective responses that they observed in frontoparietal networks, challenging ‘the classical distinction between sensory unimodal and higher-order amodal areas’. However, the interpretation of these dissociations is not straightforward. They may be the consequence of a partial dissociation of auditory and visual networks for attention [5], one of the suggestions put forward by the authors; but that is to overlook the natural presentation of the spoken narrative compared with the unnatural manner in which the written version had to be read. Thus, for example, a prominent right frontoparietal activity that was observed for the written relative to the spoken narrative was arguably a consequence of the relatively greater demand on sustained attention; in other words, activity associated with experimental design and not with language modality. We found the distribution of the invariant responses to be much more intriguing. Most prominent was a distribution of correlated activity in the midline posterior cortex and bilateral posterior inferior parietal cortex. This forms the posterior part of the so-called default mode network (DMN; Figure 1), a system classically associated with the introspective mind. It has been observed before, in another meta-analysis of language studies, one that set out to reveal the semantic system [6]. The authors of that review, and others since (e.g., [7]), have discussed how memories, semantic and personal, emotions, theory of mind, and no doubt many other mental functions are linked through the DMN. This would suggest that overlapping components of the DMN are functionally interconnected with many separate
Spotlights
Trends in Cognitive Sciences March 2014, Vol. 18, No. 3
whereas the study by Spitsyna made no such demand on the participants in their PET study. There is nothing like the threat of an examination to concentrate one’s mind – and maximize one’s brain activity. The recent result addresses the literary as opposed to simply the lingual brain. There is a longstanding and often ill-tempered debate about whether Shakespeare actually wrote, singly or as a co-author, the 37 plays attributed to him. It is argued that only a well-travelled Tudor aristocrat, versed in the ways of courtly love, would have had the experiences to write the histories, tragedies, and romantic comedies attributed to Shakespeare. Now we can speculate that some background reading and curiosity about the motivations of others, coupled with a spectacularly wellconnected DMN, made the bard immortal despite his humble origins. And we know that the DMN is as active in narrative production as it is in comprehension [10].
IPP
PCC
TRENDS in Cognitive Sciences
Figure 1. Spot the literary network: the default mode network (DMN) viewed from different angles (colors are intended for illustrative purposes only; data from [9]). The medial posterior cingulate (PCC) and inferior posterior parietal components (IPP) were implicated in linguistic processing by Regev et al. [2], but we suggest that due to the widespread connectivity of the DMN, these regions are related to higher order ‘literary’ processing.
brain systems, including those for language and semantics, and indeed this is turning out to be the case [8–10]. So why did the study of Spitsyna and colleagues [3] not reveal convergence within the DMN? The answer is it did, in a figure of statistically unthresholded analyses of the contrasts between the spoken and written narratives and their respective baseline conditions. The PET study was underpowered to reveal this activity at a thresholded level, but a further factor was likely to have been the expectations of the participants. In the study of Regev and colleagues [2] the participants knew they would have to recall the content of the narrative at the cessation of scanning,
References 1 Vigneau, M. et al. (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30, 1414–1432 2 Regev, M. et al. (2013) Selective and invariant neural responses to spoken and written narratives. J. Neurosci. 33, 15978–15988 3 Spitsyna, G. et al. (2006) Converging language streams in the human temporal lobe. J. Neurosci. 26, 7328–7336 4 Acosta-Cabronero, J. et al. (2011) Atrophy, hypometabolism and white matter abnormalities in semantic dementia tell a coherent story. Brain 134, 2025–2035 5 Braga, R.M. et al. (2013) Separable networks for top-down attention to auditory non-spatial and visuospatial modalities. Neuroimage 74, 77–86 6 Binder, J.R. et al. (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 19, 2767–2796 7 Buckner, R.L. and Carroll, D.C. (2007) Self-projection and the brain. Trends Cogn. Sci. 11, 49–57 8 Smith, S.M. et al. (2012) Temporally-independent functional modes of spontaneous brain activity. Proc. Natl. Acad. Sci. U.S.A. 109, 3131–3136 9 Braga, R.M. et al. (2013) Echoes of the brain within default mode, association, and heteromodal cortices. J. Neurosci. 33, 14031–14039 10 Awad, M. et al. (2007) A common system for the comprehension and production of narrative speech. J. Neurosci. 27, 11455–11464
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