The Roles of Left Versus Right Anterior Temporal Lobes in Conceptual Knowledge: An ALE Meta-analysis of 97 Functional Neuroimaging Studies

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The goal of cognitive neuroscience is to integrate cognitive models with knowledge about underlying neural machinery. This significant challenge was explored in relation to word reading, where sophisticated computational-cognitive models exist but have made limited contact with neural data. Using distortion-corrected functional MRI and dynamic causal modeling, we investigated the interactions between brain regions dedicated to orthographic, semantic, and phonological processing while participants read words aloud. We found that the lateral anterior temporal lobe exhibited increased activation when participants read words with irregular spellings. This area is implicated in semantic processing but has not previously been considered part of the reading network. We also found meaningful individual differences in the activation of this region: Activity was predicted by an independent measure of the degree to which participants use semantic knowledge to read. These characteristics are predicted by the connectionist Triangle Model of reading and indicate a key role for semantic knowledge in reading aloud. Premotor regions associated with phonological processing displayed the reverse characteristics. Changes in the functional connectivity of the reading network during irregular word reading also were consistent with semantic recruitment. These data support the view that reading aloud is underpinned by the joint operation of two neural pathways. They reveal that (i) the ATL is an important element of the ventral semantic pathway and (ii) the division of labor between the two routes varies according to both the properties of the words being read and individual differences in the degree to which participants rely on each route.triangle model | anterior temporal lobe | semantic reliance | reading | surface dyslexia C ognitive neuroscience offers the exciting prospect of understanding the neural basis of cognitive behaviors, a goal which requires integration of sophisticated cognitive models with knowledge about the underlying neural machinery. As a key cognitive skill, reading provides an advanced test case. Computationally implemented theories present detailed accounts of how reading is accomplished at a cognitive level (1-4). To achieve a full understanding of reading and its impairment in neurological disorders, these cognitive theories must be integrated with information about the neural basis of the reading system. However, although various studies have explored the neural basis of reading (5), the level of integration between cognitive and neural models remains limited. In the present study, we used an improved functional MRI (fMRI) protocol to test the specific predictions of an influential computational model of word reading: the connectionist "Triangle Model" (2). We were able to map specific elements of this cognitive model onto different cortical regions, thereby providing a direct link between cognitive theorizing and neural implementation. Specifically, we provide insights into the division of labor between se...

Section: Discussionsupporting

confidence: 76%

Triangulation of the neurocomputational architecture underpinning reading aloud

Hoffman

Ralph

Woollams

2015

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“…This finding adds to a growing body of literature comparing processing in the left vs. right ATL. A seminal magnetoencephalography study of semantic processing across modalities, as well as a recent largescale meta-analysis of functional imaging studies (37,39), found that ATL activation for written words or speech production is strongly left-lateralized, whereas other forms of semantic tasks (pictures, auditory words, and auditory sounds) show bilateral ATL engagement (see also ref. 19).…”

Section: Discussionmentioning

confidence: 99%

Establishing task- and modality-dependent dissociations between the semantic and default mode networks

Humphreys

Hoffman

Visser

et al. 2015

Self Cite

191

240

The default mode network (DMN) and semantic network (SN) are two of the most extensively studied systems, and both are increasingly used as clinical biomarkers in neurological studies. There are strong theoretical reasons to assume a relationship between the networks, as well as anatomical evidence that they might rely on overlapping cortical regions, such as the anterior temporal lobe (ATL) or angular gyrus (AG). Despite these strong motivations, the relationship between the two systems has received minimal attention. We directly compared the SN and DMN using a large (n = 69) distortion-corrected functional MRI (fMRI) dataset, spanning a range of semantic and nonsemantic tasks that varied input modality. The results showed that both networks fractionate depending on the semantic nature of the task, stimulus type, modality, and task difficulty. Furthermore, despite recent claims that both AG and ATL are semantic hubs, the two areas responded very differently, with results supporting the role of ATL, but not AG, in semantic representation. Specifically, the left ATL was positively activated for all semantic tasks, but deactivated during nonsemantic task performance. In contrast, the left AG was deactivated for all tasks, with the level of deactivation related to task difficulty. Thus, ATL and AG do not share a common interest in semantic tasks, but, rather, a common "disinterest" in nonsemantic tasks. The implications for the variability in the DMN, its cognitive coherence, and interpretation of resting-state fMRI data are discussed.semantic network | default mode network | distortion-corrected fMRI | anterior temporal lobe | angular gyrus T wo substantial bodies of research literature, spanning cognitive and clinical neuroscience fields, have been dedicated to exploring the function and components of the semantic network (SN) and the default mode network (DMN). The DMN is an anatomically defined network that shows task-related deactivation during many goal-directed tasks (i.e., rest > task) (1) and can be reliably delineated using techniques such as independent components analysis (ICA) of resting-state functional MRI (fMRI) (2). The SN is a fronto-temporo-parietal network that is sensitive to semantic content in comparisons of semantic tasks > rest/nonsemantic control tasks (3). Although investigations of the DMN and SN have been primarily independent of each other, there are good reasons to compare the two networks directly. First, the networks might share common cognitive functions. One prominent theory suggests that during "rest," the brain is engaged in the activation of rich conceptual representations, and thus default-mode processing places strong demands on the semantic system (4). Secondly, the DMN and SN engage some common anatomical areas. The DMN consistently includes medial prefrontal cortex, parietal areas [angular gyrus (AG), precuneus, posterior cingulate cortex (PCC)], and, somewhat more variably, the lateral anterior temporal lobe (ATL) and hippocampus (1, 5). Some of these areas are considered...

“…Frontal regions are engaged in unification operations (15), integrating lexical units into the larger context. Anterior temporal cortex is associated with conceptual object representations (16,17).…”

Section: Discussionmentioning

confidence: 99%

“…Specifically, we found that rhythmic activity in the alpha frequency range (8-12 Hz) propagates from temporal cortical areas to frontal cortical areas, and that beta frequency rhythmic activity (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) propagates in the opposite direction. These results indicate the functional relevance of rhythmic directed interactions during language processing, where interactions between areas are supported by different frequency bands, depending on the direction of the interaction.…”

mentioning

confidence: 95%

Frequency-specific directed interactions in the human brain network for language

Schoffelen

Hultén

Lam

et al. 2017

118

The brain's remarkable capacity for language requires bidirectional interactions between functionally specialized brain regions. We used magnetoencephalography to investigate interregional interactions in the brain network for language while 102 participants were reading sentences. Using Granger causality analysis, we identified inferior frontal cortex and anterior temporal regions to receive widespread input and middle temporal regions to send widespread output. This fits well with the notion that these regions play a central role in language processing. Characterization of the functional topology of this network, using data-driven matrix factorization, which allowed for partitioning into a set of subnetworks, revealed directed connections at distinct frequencies of interaction. Connections originating from temporal regions peaked at alpha frequency, whereas connections originating from frontal and parietal regions peaked at beta frequency. These findings indicate that the information flow between language-relevant brain areas, which is required for linguistic processing, may depend on the contributions of distinct brain rhythms.language | Granger causality | brain networks | magnetoencephalography T he human brain is capable of effortlessly extracting meaning from sequences of written or spoken words by means of a sophisticated interplay between dedicated neocortical regions. Neuroanatomical research has revealed a number of white-matter pathways that facilitate these interregional interactions (1). Electrophysiological research with electro-and magnetoencephalography (EEG/MEG) has revealed with high temporal precision the sequential activation of individual nodes embedded within the human brain network for language (2, 3). However, the nature of the functional interactions that enable the efficient flow of information between the nodes of this network has yet to be elucidated.One important feature of cortical interregional connections is that they are frequently reciprocal in nature (4), which implies that information can be exchanged in a bidirectional fashion. Moreover, the information flow between cortical regions may be facilitated by interregional rhythmic synchronization (5), where neuronal rhythms of specific different frequencies reflect the direction in which the information is flowing (6, 7). This bidirectional flow of information should also be a crucial feature of the neurobiological system that supports language processing. Linguistic processing is not a simple bottom-up process where incoming linguistic information (for instance, when reading a sentence) drives a sequence of activations of cortical areas that gradually transforms a string of letters into a representation of sentence and discourse meaning. Rather, contextual information, which is either already available, or built up while a sentence unfolds, can also provide top-down information, affecting the response in lower-order areas.Here, we show that interregional interactions in the human brain network for language are subserved by rhyt...