Graded and sharp transitions in semantic function in left temporal lobe.

Recent work has focussed on how patterns of functional change within the temporal lobe relate to whole-brain dimensions of intrinsic connectivity variation (Margulies et al., 2016). We examined two such 'connectivity gradients' reflecting the separation of (i) unimodal versus heteromodal and (ii) visual versus auditory-motor cortex, examining visually presented verbal associative and feature judgments, plus picture-based context and emotion generation. Functional responses along the first dimension sometimes showed graded change between modality-tuned and heteromodal cortex (in the verbal matching task), and other times showed sharp functional transitions, with deactivation at the extremes and activation in the middle of this gradient (internal generation). The second gradient revealed more visual than auditory-motor activation, regardless of content (associative, feature, context, emotion) or task process (matching/generation). We also uncovered subtle differences across each gradient for content type, which predominantly manifested as differences in relative magnitude of activation or deactivation.

Individual word representations dissociate from linguistic context along a cortical unimodal to heteromodal gradient.

Language comprehension involves multiple hierarchical processing stages across time, space, and levels of representation. When processing a word, the sensory input is transformed into increasingly abstract representations that need to be integrated with the linguistic context. Thus, language comprehension involves both input-driven as well as context-dependent processes. While neuroimaging research has traditionally focused on mapping individual brain regions to the distinct underlying processes, recent studies indicate that whole-brain distributed patterns of cortical activation might be highly relevant for cognitive functions, including language. One such pattern, based on resting-state connectivity, is the 'principal cortical gradient', which dissociates sensory from heteromodal brain regions. The present study investigated the extent to which this gradient provides an organizational principle underlying language function, using a multimodal neuroimaging dataset of functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) recordings from 102 participants during sentence reading. We found that the brain response to individual representations of a word (word length, orthographic distance, and word frequency), which reflect visual; orthographic; and lexical properties, gradually increases towards the sensory end of the gradient. Although these properties showed opposite effect directions in fMRI and MEG, their association with the sensory end of the gradient was consistent across both neuroimaging modalities. In contrast, MEG revealed that properties reflecting a word's relation to its linguistic context (semantic similarity and position within the sentence) involve the heteromodal end of the gradient to a stronger extent. This dissociation between individual word and contextual properties was stable across earlier and later time windows during word presentation, indicating interactive processing of word representations and linguistic context at opposing ends of the principal gradient. To conclude, our findings indicate that the principal gradient underlies the organization of a range of linguistic representations while supporting a gradual distinction between context-independent and context-dependent representations. Furthermore, the gradient reveals convergent patterns across neuroimaging modalities (similar location along the gradient) in the presence of divergent responses (opposite effect directions).

A tale of two gradients: differences between the left and right hemispheres predict semantic cognition.

Decomposition of whole-brain functional connectivity patterns reveals a principal gradient that captures the separation of sensorimotor cortex from heteromodal regions in the default mode network (DMN). Functional homotopy is strongest in sensorimotor areas, and weakest in heteromodal cortices, suggesting there may be differences between the left and right hemispheres (LH/RH) in the principal gradient, especially towards its apex. This study characterised hemispheric differences in the position of large-scale cortical networks along the principal gradient, and their functional significance. We collected resting-state fMRI and semantic, working memory and non-verbal reasoning performance in 175 + healthy volunteers. We then extracted the principal gradient of connectivity for each participant, tested which networks showed significant hemispheric differences on the gradient, and regressed participants' behavioural efficiency in tasks outside the scanner against interhemispheric gradient differences for each network. LH showed a higher overall principal gradient value, consistent with its role in heteromodal semantic cognition. One frontotemporal control subnetwork was linked to individual differences in semantic cognition: when it was nearer heteromodal DMN on the principal gradient in LH, participants showed more efficient semantic retrieval-and this network also showed a strong hemispheric difference in response to semantic demands but not working memory load in a separate study. In contrast, when a dorsal attention subnetwork was closer to the heteromodal end of the principal gradient in RH, participants showed better visual reasoning. Lateralization of function may reflect differences in connectivity between control and heteromodal regions in LH, and attention and visual regions in RH.

Dissociations in semantic cognition: Oscillatory evidence for opposing effects of semantic control and type of semantic relation in anterior and posterior temporal cortex.

How does the brain represent and process different types of knowledge? The Dual Hub account postulates that anterior temporal lobes (ATL) support taxonomic relationships based on shared physical features (mole - cat), while temporoparietal regions, including posterior middle temporal gyrus (pMTG), support thematic associations (mole - earth). Conversely, the Controlled Semantic Cognition account proposes that ATL supports both aspects of knowledge, while left pMTG contributes to controlled retrieval. This study used magnetoencephalography to test these contrasting predictions of functional dissociations within the temporal lobe. ATL and pMTG responded more strongly to taxonomic and thematic trials respectively, matched for behavioural performance, in line with predictions of the Dual Hub account. In addition, ATL showed a greater response to strong than weak thematic associations, while pMTG showed the opposite pattern, supporting a key prediction of the Controlled Semantic Cognition account. ATL showed a stronger response for word pairs that were more semantically coherent, either because they shared physical features (in taxonomic trials) or a strong thematic association. These effects largely coincided in time and frequency (although an early oscillatory response in ATL was specific to taxonomic trials). In contrast, pMTG showed non-overlapping effects of semantic control demands and thematic judgements: this site showed a larger oscillatory response to weak associations, when ongoing retrieval needed to be shaped to suit the task demands, and also a larger response to thematic judgements contrasted with taxonomic trials (which was reduced but not eliminated when the thematic trials were easier). Consequently, time-sensitive neuroimaging supports a complex pattern of functional dissociations within the left temporal lobe, which reflects both coherence versus control and distinctive oscillatory responses for taxonomic overlap (in ATL) and thematic relations (in pMTG).

Degrees of lateralisation in semantic cognition: Evidence from intrinsic connectivity.

The semantic network is thought to include multiple components, including heteromodal conceptual representations and semantic control processes that shape retrieval to suit the circumstances. Much of this network is strongly left-lateralised; however, work to date has not considered whether separable components of semantic cognition have different degrees of lateralisation. This study examined intrinsic connectivity of four regions implicated in heteromodal semantic cognition, identified using large scale meta-analyses: two sites which have been argued to act as heteromodal semantic hubs in anterior temporal lobe (ATL) and angular gyrus (AG); and two sites implicated in semantic control in inferior frontal (IFG) and posterior middle temporal gyri (pMTG). We compared the intrinsic connectivity of these sites in left hemisphere (LH) and right hemisphere (RH), and linked individual differences in the strength of within- and between-hemisphere connectivity from left-lateralised seeds to performance on semantic tasks, in a sample of 196 healthy volunteers. ATL showed more symmetrical patterns of intrinsic connectivity than the other three sites. The connectivity between IFG and pMTG was stronger in the LH than the RH, suggesting that the semantic control network is strongly left-lateralised. The degree of hemispheric lateralisation also predicted behaviour: participants with stronger intrinsic connectivity within the LH had better semantic performance, while those with stronger intrinsic connectivity between left pMTG and homotopes of semantic regions in the RH performed more poorly on judgements of weak associations, which require greater control. Stronger connectivity between left AG and visual cortex was also linked to poorer perceptual performance. Overall, our results show that hemispheric lateralisation is particularly important for the semantic control network, and that this lateralisation has contrasting functional consequences for the retrieval of dominant and subordinate aspects of knowledge.

The structural basis of semantic control: Evidence from individual differences in cortical thickness.

Semantic control allows us to shape our conceptual retrieval to suit the circumstances in a flexible way. Tasks requiring semantic control activate a large-scale network including left inferior prefrontal gyrus (IFG) and posterior middle temporal gyrus (pMTG) - this network responds when retrieval is focussed on weak as opposed to dominant associations. However, little is known about the biological basis of individual differences in this cognitive capacity: regions that are commonly activated in task-based fMRI may not relate to variation in controlled retrieval. The current study combined analyses of MRI-based cortical thickness with resting-state fMRI connectivity to identify structural markers of individual differences in semantic control. We found that participants who performed relatively well on tests of controlled semantic retrieval showed increased structural covariance between left pMTG and left anterior middle frontal gyrus (aMFG). This pattern of structural covariance was specific to semantic control and did not predict performance when harder non-semantic judgements were contrasted with easier semantic judgements. The intrinsic functional connectivity of these two regions forming a structural covariance network overlapped with previously-described semantic control regions, including bilateral IFG and intraparietal sulcus, and left posterior temporal cortex. These results add to our knowledge of the neural basis of semantic control in three ways: (i) Semantic control performance was predicted by the structural covariance network of left pMTG, a site that is less consistently activated than left IFG across studies. (ii) Our results provide further evidence that semantic control is at least partially separable from domain-general executive control. (iii) More flexible patterns of memory retrieval occurred when pMTG co-varied with distant regions in aMFG, as opposed to nearby visual, temporal or parietal lobe regions, providing further evidence that left prefrontal and posterior temporal areas form a distributed network for semantic control.